diff --git a/.github/workflows/version-bump.yml b/.github/workflows/version-bump.yml
index 8e126e1da60..680441a8eca 100644
--- a/.github/workflows/version-bump.yml
+++ b/.github/workflows/version-bump.yml
@@ -71,7 +71,7 @@ jobs:
         uses: actions/checkout@8ade135a41bc03ea155e62e844d188df1ea18608 # v4.1.0
         with:
           repository: bitwarden/clients
-          ref: master
+          ref: main
           token: ${{ steps.retrieve-secrets.outputs.github-pat-bitwarden-devops-bot-repo-scope }}
 
       - name: Import GPG key
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 3d6f00ec10f..f760ee22e62 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -673,7 +673,7 @@ class OverlayBackground implements OverlayBackgroundInterface {
    */
   private setupExtensionMessageListeners() {
     BrowserApi.messageListener("overlay.background", this.handleExtensionMessage);
-    chrome.runtime.onConnect.addListener(this.handlePortOnConnect);
+    BrowserApi.addListener(chrome.runtime.onConnect, this.handlePortOnConnect);
   }
 
   /**
diff --git a/apps/browser/src/autofill/background/service_factories/autofill-service.factory.ts b/apps/browser/src/autofill/background/service_factories/autofill-service.factory.ts
index acd9be2a8ea..972a2421cbb 100644
--- a/apps/browser/src/autofill/background/service_factories/autofill-service.factory.ts
+++ b/apps/browser/src/autofill/background/service_factories/autofill-service.factory.ts
@@ -10,6 +10,10 @@ import {
   settingsServiceFactory,
   SettingsServiceInitOptions,
 } from "../../../background/service-factories/settings-service.factory";
+import {
+  configServiceFactory,
+  ConfigServiceInitOptions,
+} from "../../../platform/background/service-factories/config-service.factory";
 import {
   CachedServices,
   factory,
@@ -43,7 +47,8 @@ export type AutoFillServiceInitOptions = AutoFillServiceOptions &
   EventCollectionServiceInitOptions &
   LogServiceInitOptions &
   SettingsServiceInitOptions &
-  UserVerificationServiceInitOptions;
+  UserVerificationServiceInitOptions &
+  ConfigServiceInitOptions;
 
 export function autofillServiceFactory(
   cache: { autofillService?: AbstractAutoFillService } & CachedServices,
@@ -62,6 +67,7 @@ export function autofillServiceFactory(
         await logServiceFactory(cache, opts),
         await settingsServiceFactory(cache, opts),
         await userVerificationServiceFactory(cache, opts),
+        await configServiceFactory(cache, opts),
       ),
   );
 }
diff --git a/apps/browser/src/autofill/background/tabs.background.spec.ts b/apps/browser/src/autofill/background/tabs.background.spec.ts
index b3de1e96ce3..304d43bd143 100644
--- a/apps/browser/src/autofill/background/tabs.background.spec.ts
+++ b/apps/browser/src/autofill/background/tabs.background.spec.ts
@@ -15,7 +15,7 @@ import OverlayBackground from "./overlay.background";
 import TabsBackground from "./tabs.background";
 
 describe("TabsBackground", () => {
-  let tabsBackgorund: TabsBackground;
+  let tabsBackground: TabsBackground;
   const mainBackground = mock<MainBackground>({
     messagingService: {
       send: jest.fn(),
@@ -25,7 +25,7 @@ describe("TabsBackground", () => {
   const overlayBackground = mock<OverlayBackground>();
 
   beforeEach(() => {
-    tabsBackgorund = new TabsBackground(mainBackground, notificationBackground, overlayBackground);
+    tabsBackground = new TabsBackground(mainBackground, notificationBackground, overlayBackground);
   });
 
   afterEach(() => {
@@ -35,11 +35,11 @@ describe("TabsBackground", () => {
   describe("init", () => {
     it("sets up a window on focusChanged listener", () => {
       const handleWindowOnFocusChangedSpy = jest.spyOn(
-        tabsBackgorund as any,
+        tabsBackground as any,
         "handleWindowOnFocusChanged",
       );
 
-      tabsBackgorund.init();
+      tabsBackground.init();
 
       expect(chrome.windows.onFocusChanged.addListener).toHaveBeenCalledWith(
         handleWindowOnFocusChangedSpy,
@@ -49,7 +49,7 @@ describe("TabsBackground", () => {
 
   describe("tab event listeners", () => {
     beforeEach(() => {
-      tabsBackgorund.init();
+      tabsBackground["setupTabEventListeners"]();
     });
 
     describe("window onFocusChanged event", () => {
@@ -64,7 +64,7 @@ describe("TabsBackground", () => {
         triggerWindowOnFocusedChangedEvent(10);
         await flushPromises();
 
-        expect(tabsBackgorund["focusedWindowId"]).toBe(10);
+        expect(tabsBackground["focusedWindowId"]).toBe(10);
       });
 
       it("updates the current tab data", async () => {
@@ -144,7 +144,7 @@ describe("TabsBackground", () => {
 
       beforeEach(() => {
         mainBackground.onUpdatedRan = false;
-        tabsBackgorund["focusedWindowId"] = focusedWindowId;
+        tabsBackground["focusedWindowId"] = focusedWindowId;
         tab = mock<chrome.tabs.Tab>({
           windowId: focusedWindowId,
           active: true,
diff --git a/apps/browser/src/autofill/background/tabs.background.ts b/apps/browser/src/autofill/background/tabs.background.ts
index b095f99ce20..8b4cb356a7e 100644
--- a/apps/browser/src/autofill/background/tabs.background.ts
+++ b/apps/browser/src/autofill/background/tabs.background.ts
@@ -20,6 +20,14 @@ export default class TabsBackground {
       return;
     }
 
+    this.updateCurrentTabData();
+    this.setupTabEventListeners();
+  }
+
+  /**
+   * Sets up the tab and window event listeners.
+   */
+  private setupTabEventListeners() {
     chrome.windows.onFocusChanged.addListener(this.handleWindowOnFocusChanged);
     chrome.tabs.onActivated.addListener(this.handleTabOnActivated);
     chrome.tabs.onReplaced.addListener(this.handleTabOnReplaced);
@@ -33,7 +41,7 @@ export default class TabsBackground {
    * @param windowId - The ID of the window that was focused.
    */
   private handleWindowOnFocusChanged = async (windowId: number) => {
-    if (!windowId) {
+    if (windowId == null || windowId < 0) {
       return;
     }
 
@@ -116,8 +124,10 @@ export default class TabsBackground {
    * for the current tab. Also updates the overlay ciphers.
    */
   private updateCurrentTabData = async () => {
-    await this.main.refreshBadge();
-    await this.main.refreshMenu();
-    await this.overlayBackground.updateOverlayCiphers();
+    await Promise.all([
+      this.main.refreshBadge(),
+      this.main.refreshMenu(),
+      this.overlayBackground.updateOverlayCiphers(),
+    ]);
   };
 }
diff --git a/apps/browser/src/autofill/content/abstractions/autofill-init.ts b/apps/browser/src/autofill/content/abstractions/autofill-init.ts
index 139099a4d58..91866ffa0bb 100644
--- a/apps/browser/src/autofill/content/abstractions/autofill-init.ts
+++ b/apps/browser/src/autofill/content/abstractions/autofill-init.ts
@@ -17,6 +17,7 @@ type AutofillExtensionMessage = {
     direction?: "previous" | "next";
     isOpeningFullOverlay?: boolean;
     forceCloseOverlay?: boolean;
+    autofillOverlayVisibility?: number;
   };
 };
 
@@ -34,10 +35,12 @@ type AutofillExtensionMessageHandlers = {
   updateIsOverlayCiphersPopulated: ({ message }: AutofillExtensionMessageParam) => void;
   bgUnlockPopoutOpened: () => void;
   bgVaultItemRepromptPopoutOpened: () => void;
+  updateAutofillOverlayVisibility: ({ message }: AutofillExtensionMessageParam) => void;
 };
 
 interface AutofillInit {
   init(): void;
+  destroy(): void;
 }
 
 export { AutofillExtensionMessage, AutofillExtensionMessageHandlers, AutofillInit };
diff --git a/apps/browser/src/autofill/content/autofill-init.spec.ts b/apps/browser/src/autofill/content/autofill-init.spec.ts
index 1524fdce100..ecf67740183 100644
--- a/apps/browser/src/autofill/content/autofill-init.spec.ts
+++ b/apps/browser/src/autofill/content/autofill-init.spec.ts
@@ -6,7 +6,7 @@ import { flushPromises, sendExtensionRuntimeMessage } from "../jest/testing-util
 import AutofillPageDetails from "../models/autofill-page-details";
 import AutofillScript from "../models/autofill-script";
 import AutofillOverlayContentService from "../services/autofill-overlay-content.service";
-import { RedirectFocusDirection } from "../utils/autofill-overlay.enum";
+import { AutofillOverlayVisibility, RedirectFocusDirection } from "../utils/autofill-overlay.enum";
 
 import { AutofillExtensionMessage } from "./abstractions/autofill-init";
 import AutofillInit from "./autofill-init";
@@ -16,6 +16,11 @@ describe("AutofillInit", () => {
   const autofillOverlayContentService = mock<AutofillOverlayContentService>();
 
   beforeEach(() => {
+    chrome.runtime.connect = jest.fn().mockReturnValue({
+      onDisconnect: {
+        addListener: jest.fn(),
+      },
+    });
     autofillInit = new AutofillInit(autofillOverlayContentService);
   });
 
@@ -477,6 +482,57 @@ describe("AutofillInit", () => {
           expect(autofillInit["removeAutofillOverlay"]).toHaveBeenCalled();
         });
       });
+
+      describe("updateAutofillOverlayVisibility", () => {
+        beforeEach(() => {
+          autofillInit["autofillOverlayContentService"].autofillOverlayVisibility =
+            AutofillOverlayVisibility.OnButtonClick;
+        });
+
+        it("skips attempting to update the overlay visibility if the autofillOverlayVisibility data value is not present", () => {
+          sendExtensionRuntimeMessage({
+            command: "updateAutofillOverlayVisibility",
+            data: {},
+          });
+
+          expect(autofillInit["autofillOverlayContentService"].autofillOverlayVisibility).toEqual(
+            AutofillOverlayVisibility.OnButtonClick,
+          );
+        });
+
+        it("updates the overlay visibility value", () => {
+          const message = {
+            command: "updateAutofillOverlayVisibility",
+            data: {
+              autofillOverlayVisibility: AutofillOverlayVisibility.Off,
+            },
+          };
+
+          sendExtensionRuntimeMessage(message);
+
+          expect(autofillInit["autofillOverlayContentService"].autofillOverlayVisibility).toEqual(
+            message.data.autofillOverlayVisibility,
+          );
+        });
+      });
+    });
+  });
+
+  describe("destroy", () => {
+    it("removes the extension message listeners", () => {
+      autofillInit.destroy();
+
+      expect(chrome.runtime.onMessage.removeListener).toHaveBeenCalledWith(
+        autofillInit["handleExtensionMessage"],
+      );
+    });
+
+    it("destroys the collectAutofillContentService", () => {
+      jest.spyOn(autofillInit["collectAutofillContentService"], "destroy");
+
+      autofillInit.destroy();
+
+      expect(autofillInit["collectAutofillContentService"].destroy).toHaveBeenCalled();
     });
   });
 });
diff --git a/apps/browser/src/autofill/content/autofill-init.ts b/apps/browser/src/autofill/content/autofill-init.ts
index 9b23305377c..5a2ec3dd397 100644
--- a/apps/browser/src/autofill/content/autofill-init.ts
+++ b/apps/browser/src/autofill/content/autofill-init.ts
@@ -26,6 +26,7 @@ class AutofillInit implements AutofillInitInterface {
     updateIsOverlayCiphersPopulated: ({ message }) => this.updateIsOverlayCiphersPopulated(message),
     bgUnlockPopoutOpened: () => this.blurAndRemoveOverlay(),
     bgVaultItemRepromptPopoutOpened: () => this.blurAndRemoveOverlay(),
+    updateAutofillOverlayVisibility: ({ message }) => this.updateAutofillOverlayVisibility(message),
   };
 
   /**
@@ -214,6 +215,19 @@ class AutofillInit implements AutofillInitInterface {
     );
   }
 
+  /**
+   * Updates the autofill overlay visibility.
+   *
+   * @param data - Contains the autoFillOverlayVisibility value
+   */
+  private updateAutofillOverlayVisibility({ data }: AutofillExtensionMessage) {
+    if (!this.autofillOverlayContentService || isNaN(data?.autofillOverlayVisibility)) {
+      return;
+    }
+
+    this.autofillOverlayContentService.autofillOverlayVisibility = data?.autofillOverlayVisibility;
+  }
+
   /**
    * Sets up the extension message listeners for the content script.
    */
@@ -247,6 +261,16 @@ class AutofillInit implements AutofillInitInterface {
     Promise.resolve(messageResponse).then((response) => sendResponse(response));
     return true;
   };
+
+  /**
+   * Handles destroying the autofill init content script. Removes all
+   * listeners, timeouts, and object instances to prevent memory leaks.
+   */
+  destroy() {
+    chrome.runtime.onMessage.removeListener(this.handleExtensionMessage);
+    this.collectAutofillContentService.destroy();
+    this.autofillOverlayContentService?.destroy();
+  }
 }
 
 export default AutofillInit;
diff --git a/apps/browser/src/autofill/content/autofiller.ts b/apps/browser/src/autofill/content/autofiller.ts
index 7f58e72c7d3..c3a2f7f5793 100644
--- a/apps/browser/src/autofill/content/autofiller.ts
+++ b/apps/browser/src/autofill/content/autofiller.ts
@@ -1,3 +1,5 @@
+import { getFromLocalStorage, setupExtensionDisconnectAction } from "../utils";
+
 if (document.readyState === "loading") {
   document.addEventListener("DOMContentLoaded", loadAutofiller);
 } else {
@@ -8,27 +10,30 @@ function loadAutofiller() {
   let pageHref: string = null;
   let filledThisHref = false;
   let delayFillTimeout: number;
-
-  const activeUserIdKey = "activeUserId";
-  let activeUserId: string;
-
-  chrome.storage.local.get(activeUserIdKey, (obj: any) => {
-    if (obj == null || obj[activeUserIdKey] == null) {
-      return;
-    }
-    activeUserId = obj[activeUserIdKey];
-  });
-
-  chrome.storage.local.get(activeUserId, (obj: any) => {
-    if (obj?.[activeUserId]?.settings?.enableAutoFillOnPageLoad === true) {
-      setInterval(() => doFillIfNeeded(), 500);
-    }
-  });
-  chrome.runtime.onMessage.addListener((msg, sender, sendResponse) => {
-    if (msg.command === "fillForm" && pageHref === msg.url) {
+  let doFillInterval: NodeJS.Timeout;
+  const handleExtensionDisconnect = () => {
+    clearDoFillInterval();
+    clearDelayFillTimeout();
+  };
+  const handleExtensionMessage = (message: any) => {
+    if (message.command === "fillForm" && pageHref === message.url) {
       filledThisHref = true;
     }
-  });
+  };
+
+  setupExtensionEventListeners();
+  triggerUserFillOnLoad();
+
+  async function triggerUserFillOnLoad() {
+    const activeUserIdKey = "activeUserId";
+    const userKeyStorage = await getFromLocalStorage(activeUserIdKey);
+    const activeUserId = userKeyStorage[activeUserIdKey];
+    const activeUserStorage = await getFromLocalStorage(activeUserId);
+    if (activeUserStorage?.[activeUserId]?.settings?.enableAutoFillOnPageLoad === true) {
+      clearDoFillInterval();
+      doFillInterval = setInterval(() => doFillIfNeeded(), 500);
+    }
+  }
 
   function doFillIfNeeded(force = false) {
     if (force || pageHref !== window.location.href) {
@@ -36,9 +41,7 @@ function loadAutofiller() {
         // Some websites are slow and rendering all page content. Try to fill again later
         // if we haven't already.
         filledThisHref = false;
-        if (delayFillTimeout != null) {
-          window.clearTimeout(delayFillTimeout);
-        }
+        clearDelayFillTimeout();
         delayFillTimeout = window.setTimeout(() => {
           if (!filledThisHref) {
             doFillIfNeeded(true);
@@ -55,4 +58,21 @@ function loadAutofiller() {
       chrome.runtime.sendMessage(msg);
     }
   }
+
+  function clearDoFillInterval() {
+    if (doFillInterval) {
+      window.clearInterval(doFillInterval);
+    }
+  }
+
+  function clearDelayFillTimeout() {
+    if (delayFillTimeout) {
+      window.clearTimeout(delayFillTimeout);
+    }
+  }
+
+  function setupExtensionEventListeners() {
+    setupExtensionDisconnectAction(handleExtensionDisconnect);
+    chrome.runtime.onMessage.addListener(handleExtensionMessage);
+  }
 }
diff --git a/apps/browser/src/autofill/content/bootstrap-autofill-overlay.ts b/apps/browser/src/autofill/content/bootstrap-autofill-overlay.ts
index 5bc9fb1718f..ab21e367c29 100644
--- a/apps/browser/src/autofill/content/bootstrap-autofill-overlay.ts
+++ b/apps/browser/src/autofill/content/bootstrap-autofill-overlay.ts
@@ -1,4 +1,5 @@
 import AutofillOverlayContentService from "../services/autofill-overlay-content.service";
+import { setupAutofillInitDisconnectAction } from "../utils";
 
 import AutofillInit from "./autofill-init";
 
@@ -6,6 +7,8 @@ import AutofillInit from "./autofill-init";
   if (!windowContext.bitwardenAutofillInit) {
     const autofillOverlayContentService = new AutofillOverlayContentService();
     windowContext.bitwardenAutofillInit = new AutofillInit(autofillOverlayContentService);
+    setupAutofillInitDisconnectAction(windowContext);
+
     windowContext.bitwardenAutofillInit.init();
   }
 })(window);
diff --git a/apps/browser/src/autofill/content/bootstrap-autofill.ts b/apps/browser/src/autofill/content/bootstrap-autofill.ts
index 3264c77ea0e..f98d4bc1d72 100644
--- a/apps/browser/src/autofill/content/bootstrap-autofill.ts
+++ b/apps/browser/src/autofill/content/bootstrap-autofill.ts
@@ -1,8 +1,12 @@
+import { setupAutofillInitDisconnectAction } from "../utils";
+
 import AutofillInit from "./autofill-init";
 
 (function (windowContext) {
   if (!windowContext.bitwardenAutofillInit) {
     windowContext.bitwardenAutofillInit = new AutofillInit();
+    setupAutofillInitDisconnectAction(windowContext);
+
     windowContext.bitwardenAutofillInit.init();
   }
 })(window);
diff --git a/apps/browser/src/autofill/content/message_handler.ts b/apps/browser/src/autofill/content/message_handler.ts
index 9bf48e3b17d..7b52aeb3556 100644
--- a/apps/browser/src/autofill/content/message_handler.ts
+++ b/apps/browser/src/autofill/content/message_handler.ts
@@ -1,31 +1,4 @@
-window.addEventListener(
-  "message",
-  (event) => {
-    if (event.source !== window) {
-      return;
-    }
-
-    if (event.data.command && event.data.command === "authResult") {
-      chrome.runtime.sendMessage({
-        command: event.data.command,
-        code: event.data.code,
-        state: event.data.state,
-        lastpass: event.data.lastpass,
-        referrer: event.source.location.hostname,
-      });
-    }
-
-    if (event.data.command && event.data.command === "webAuthnResult") {
-      chrome.runtime.sendMessage({
-        command: event.data.command,
-        data: event.data.data,
-        remember: event.data.remember,
-        referrer: event.source.location.hostname,
-      });
-    }
-  },
-  false,
-);
+import { setupExtensionDisconnectAction } from "../utils";
 
 const forwardCommands = [
   "bgUnlockPopoutOpened",
@@ -34,8 +7,59 @@ const forwardCommands = [
   "addedCipher",
 ];
 
-chrome.runtime.onMessage.addListener((event) => {
-  if (forwardCommands.includes(event.command)) {
-    chrome.runtime.sendMessage(event);
+/**
+ * Handles sending extension messages to the background
+ * script based on window messages from the page.
+ *
+ * @param event - Window message event
+ */
+const handleWindowMessage = (event: MessageEvent) => {
+  if (event.source !== window) {
+    return;
   }
-});
+
+  if (event.data.command && event.data.command === "authResult") {
+    chrome.runtime.sendMessage({
+      command: event.data.command,
+      code: event.data.code,
+      state: event.data.state,
+      lastpass: event.data.lastpass,
+      referrer: event.source.location.hostname,
+    });
+  }
+
+  if (event.data.command && event.data.command === "webAuthnResult") {
+    chrome.runtime.sendMessage({
+      command: event.data.command,
+      data: event.data.data,
+      remember: event.data.remember,
+      referrer: event.source.location.hostname,
+    });
+  }
+};
+
+/**
+ * Handles forwarding any commands that need to trigger
+ * an action from one service of the extension background
+ * to another.
+ *
+ * @param message - Message from the extension
+ */
+const handleExtensionMessage = (message: any) => {
+  if (forwardCommands.includes(message.command)) {
+    chrome.runtime.sendMessage(message);
+  }
+};
+
+/**
+ * Handles cleaning up any event listeners that were
+ * added to the window or extension.
+ */
+const handleExtensionDisconnect = () => {
+  window.removeEventListener("message", handleWindowMessage);
+  chrome.runtime.onMessage.removeListener(handleExtensionMessage);
+};
+
+window.addEventListener("message", handleWindowMessage, false);
+chrome.runtime.onMessage.addListener(handleExtensionMessage);
+setupExtensionDisconnectAction(handleExtensionDisconnect);
diff --git a/apps/browser/src/autofill/content/notification-bar.ts b/apps/browser/src/autofill/content/notification-bar.ts
index 92e8f599385..6c3f3561e5b 100644
--- a/apps/browser/src/autofill/content/notification-bar.ts
+++ b/apps/browser/src/autofill/content/notification-bar.ts
@@ -4,6 +4,7 @@ import AddLoginRuntimeMessage from "../notification/models/add-login-runtime-mes
 import ChangePasswordRuntimeMessage from "../notification/models/change-password-runtime-message";
 import { FormData } from "../services/abstractions/autofill.service";
 import { GlobalSettings, UserSettings } from "../types";
+import { getFromLocalStorage, setupExtensionDisconnectAction } from "../utils";
 
 interface HTMLElementWithFormOpId extends HTMLElement {
   formOpId: string;
@@ -122,6 +123,8 @@ async function loadNotificationBar() {
     }
   }
 
+  setupExtensionDisconnectAction(handleExtensionDisconnection);
+
   if (!showNotificationBar) {
     return;
   }
@@ -999,11 +1002,23 @@ async function loadNotificationBar() {
     return theEl === document;
   }
 
+  function handleExtensionDisconnection(port: chrome.runtime.Port) {
+    closeBar(false);
+    clearTimeout(domObservationCollectTimeoutId);
+    clearTimeout(collectPageDetailsTimeoutId);
+    clearTimeout(handlePageChangeTimeoutId);
+    observer?.disconnect();
+    observer = null;
+    watchedForms.forEach((wf: WatchedForm) => {
+      const form = wf.formEl;
+      form.removeEventListener("submit", formSubmitted, false);
+      const submitButton = getSubmitButton(
+        form,
+        unionSets(logInButtonNames, changePasswordButtonNames),
+      );
+      submitButton?.removeEventListener("click", formSubmitted, false);
+    });
+  }
+
   // End Helper Functions
 }
-
-async function getFromLocalStorage(keys: string | string[]): Promise<Record<string, any>> {
-  return new Promise((resolve) => {
-    chrome.storage.local.get(keys, (storage: Record<string, any>) => resolve(storage));
-  });
-}
diff --git a/apps/browser/src/autofill/enums/autofill-port.enums.ts b/apps/browser/src/autofill/enums/autofill-port.enums.ts
new file mode 100644
index 00000000000..e5b8f17aad5
--- /dev/null
+++ b/apps/browser/src/autofill/enums/autofill-port.enums.ts
@@ -0,0 +1,5 @@
+const AutofillPort = {
+  InjectedScript: "autofill-injected-script-port",
+} as const;
+
+export { AutofillPort };
diff --git a/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts b/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts
index 20f5aa830fc..c878f961f1c 100644
--- a/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts
+++ b/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts
@@ -1,5 +1,5 @@
 import { EVENTS } from "../../constants";
-import { setElementStyles } from "../../utils/utils";
+import { setElementStyles } from "../../utils";
 import {
   BackgroundPortMessageHandlers,
   AutofillOverlayIframeService as AutofillOverlayIframeServiceInterface,
@@ -166,9 +166,10 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
 
     this.updateElementStyles(this.iframe, { opacity: "0", height: "0px", display: "block" });
     globalThis.removeEventListener("message", this.handleWindowMessage);
-    this.port.onMessage.removeListener(this.handlePortMessage);
-    this.port.onDisconnect.removeListener(this.handlePortDisconnect);
-    this.port.disconnect();
+    this.unobserveIframe();
+    this.port?.onMessage.removeListener(this.handlePortMessage);
+    this.port?.onDisconnect.removeListener(this.handlePortDisconnect);
+    this.port?.disconnect();
     this.port = null;
   };
 
@@ -369,7 +370,7 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
    * Unobserves the iframe element for mutations to its style attribute.
    */
   private unobserveIframe() {
-    this.iframeMutationObserver.disconnect();
+    this.iframeMutationObserver?.disconnect();
   }
 
   /**
diff --git a/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts b/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts
index 94c0772fd2b..bfb57087452 100644
--- a/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts
+++ b/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts
@@ -3,8 +3,8 @@ import "lit/polyfill-support.js";
 import { AuthenticationStatus } from "@bitwarden/common/auth/enums/authentication-status";
 
 import { EVENTS } from "../../../constants";
+import { buildSvgDomElement } from "../../../utils";
 import { logoIcon, logoLockedIcon } from "../../../utils/svg-icons";
-import { buildSvgDomElement } from "../../../utils/utils";
 import {
   InitAutofillOverlayButtonMessage,
   OverlayButtonWindowMessageHandlers,
diff --git a/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts b/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts
index 053fddb9c13..3f13061a0ed 100644
--- a/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts
+++ b/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts
@@ -4,8 +4,8 @@ import { AuthenticationStatus } from "@bitwarden/common/auth/enums/authenticatio
 
 import { OverlayCipherData } from "../../../background/abstractions/overlay.background";
 import { EVENTS } from "../../../constants";
+import { buildSvgDomElement } from "../../../utils";
 import { globeIcon, lockIcon, plusIcon, viewCipherIcon } from "../../../utils/svg-icons";
-import { buildSvgDomElement } from "../../../utils/utils";
 import {
   InitAutofillOverlayListMessage,
   OverlayListWindowMessageHandlers,
diff --git a/apps/browser/src/autofill/popup/settings/autofill.component.ts b/apps/browser/src/autofill/popup/settings/autofill.component.ts
index d9038b0eb27..728b74bc90a 100644
--- a/apps/browser/src/autofill/popup/settings/autofill.component.ts
+++ b/apps/browser/src/autofill/popup/settings/autofill.component.ts
@@ -10,6 +10,7 @@ import { UriMatchType } from "@bitwarden/common/vault/enums";
 
 import { BrowserApi } from "../../../platform/browser/browser-api";
 import { flagEnabled } from "../../../platform/flags";
+import { AutofillService } from "../../services/abstractions/autofill.service";
 import { AutofillOverlayVisibility } from "../../utils/autofill-overlay.enum";
 
 @Component({
@@ -35,6 +36,7 @@ export class AutofillComponent implements OnInit {
     private platformUtilsService: PlatformUtilsService,
     private configService: ConfigServiceAbstraction,
     private settingsService: SettingsService,
+    private autofillService: AutofillService,
   ) {
     this.autoFillOverlayVisibilityOptions = [
       {
@@ -86,7 +88,10 @@ export class AutofillComponent implements OnInit {
   }
 
   async updateAutoFillOverlayVisibility() {
+    const previousAutoFillOverlayVisibility =
+      await this.settingsService.getAutoFillOverlayVisibility();
     await this.settingsService.setAutoFillOverlayVisibility(this.autoFillOverlayVisibility);
+    await this.handleUpdatingAutofillOverlayContentScripts(previousAutoFillOverlayVisibility);
   }
 
   async updateAutoFillOnPageLoad() {
@@ -144,4 +149,25 @@ export class AutofillComponent implements OnInit {
     event.preventDefault();
     BrowserApi.createNewTab(this.disablePasswordManagerLink);
   }
+
+  private async handleUpdatingAutofillOverlayContentScripts(
+    previousAutoFillOverlayVisibility: number,
+  ) {
+    const autofillOverlayPreviouslyDisabled =
+      previousAutoFillOverlayVisibility === AutofillOverlayVisibility.Off;
+    const autofillOverlayCurrentlyDisabled =
+      this.autoFillOverlayVisibility === AutofillOverlayVisibility.Off;
+
+    if (!autofillOverlayPreviouslyDisabled && !autofillOverlayCurrentlyDisabled) {
+      const tabs = await BrowserApi.tabsQuery({});
+      tabs.forEach((tab) =>
+        BrowserApi.tabSendMessageData(tab, "updateAutofillOverlayVisibility", {
+          autofillOverlayVisibility: this.autoFillOverlayVisibility,
+        }),
+      );
+      return;
+    }
+
+    await this.autofillService.reloadAutofillScripts();
+  }
 }
diff --git a/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts b/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts
index ac7d55a54d4..ec594ac829f 100644
--- a/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts
@@ -14,6 +14,7 @@ interface AutofillOverlayContentService {
   isCurrentlyFilling: boolean;
   isOverlayCiphersPopulated: boolean;
   pageDetailsUpdateRequired: boolean;
+  autofillOverlayVisibility: number;
   init(): void;
   setupAutofillOverlayListenerOnField(
     autofillFieldElement: ElementWithOpId<FormFieldElement>,
@@ -27,6 +28,7 @@ interface AutofillOverlayContentService {
   redirectOverlayFocusOut(direction: "previous" | "next"): void;
   focusMostRecentOverlayField(): void;
   blurMostRecentOverlayField(): void;
+  destroy(): void;
 }
 
 export { OpenAutofillOverlayOptions, AutofillOverlayContentService };
diff --git a/apps/browser/src/autofill/services/abstractions/autofill.service.ts b/apps/browser/src/autofill/services/abstractions/autofill.service.ts
index a0959db72cb..c44e3adf7c9 100644
--- a/apps/browser/src/autofill/services/abstractions/autofill.service.ts
+++ b/apps/browser/src/autofill/services/abstractions/autofill.service.ts
@@ -44,10 +44,12 @@ export interface GenerateFillScriptOptions {
 }
 
 export abstract class AutofillService {
+  loadAutofillScriptsOnInstall: () => Promise<void>;
+  reloadAutofillScripts: () => Promise<void>;
   injectAutofillScripts: (
-    sender: chrome.runtime.MessageSender,
-    autofillV2?: boolean,
-    autofillOverlay?: boolean,
+    tab: chrome.tabs.Tab,
+    frameId?: number,
+    triggeringOnPageLoad?: boolean,
   ) => Promise<void>;
   getFormsWithPasswordFields: (pageDetails: AutofillPageDetails) => FormData[];
   doAutoFill: (options: AutoFillOptions) => Promise<string | null>;
diff --git a/apps/browser/src/autofill/services/abstractions/collect-autofill-content.service.ts b/apps/browser/src/autofill/services/abstractions/collect-autofill-content.service.ts
index 78befa7bc61..46ad615059a 100644
--- a/apps/browser/src/autofill/services/abstractions/collect-autofill-content.service.ts
+++ b/apps/browser/src/autofill/services/abstractions/collect-autofill-content.service.ts
@@ -22,6 +22,7 @@ interface CollectAutofillContentService {
     filterCallback: CallableFunction,
     isObservingShadowRoot?: boolean,
   ): Node[];
+  destroy(): void;
 }
 
 export {
diff --git a/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts b/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts
index 7753a4b2672..f3aa77258fe 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts
@@ -1609,4 +1609,100 @@ describe("AutofillOverlayContentService", () => {
       expect(autofillOverlayContentService["removeAutofillOverlay"]).toHaveBeenCalled();
     });
   });
+
+  describe("destroy", () => {
+    let autofillFieldElement: ElementWithOpId<FormFieldElement>;
+    let autofillFieldData: AutofillField;
+
+    beforeEach(() => {
+      document.body.innerHTML = `
+      <form id="validFormId">
+        <input type="text" id="username-field" placeholder="username" />
+        <input type="password" id="password-field" placeholder="password" />
+      </form>
+      `;
+
+      autofillFieldElement = document.getElementById(
+        "username-field",
+      ) as ElementWithOpId<FormFieldElement>;
+      autofillFieldElement.opid = "op-1";
+      autofillFieldData = createAutofillFieldMock({
+        opid: "username-field",
+        form: "validFormId",
+        placeholder: "username",
+        elementNumber: 1,
+      });
+      autofillOverlayContentService.setupAutofillOverlayListenerOnField(
+        autofillFieldElement,
+        autofillFieldData,
+      );
+      autofillOverlayContentService["mostRecentlyFocusedField"] = autofillFieldElement;
+    });
+
+    it("disconnects all mutation observers", () => {
+      autofillOverlayContentService["setupMutationObserver"]();
+      jest.spyOn(autofillOverlayContentService["bodyElementMutationObserver"], "disconnect");
+      jest.spyOn(autofillOverlayContentService["documentElementMutationObserver"], "disconnect");
+
+      autofillOverlayContentService.destroy();
+
+      expect(
+        autofillOverlayContentService["documentElementMutationObserver"].disconnect,
+      ).toHaveBeenCalled();
+      expect(
+        autofillOverlayContentService["bodyElementMutationObserver"].disconnect,
+      ).toHaveBeenCalled();
+    });
+
+    it("clears the user interaction event timeout", () => {
+      jest.spyOn(autofillOverlayContentService as any, "clearUserInteractionEventTimeout");
+
+      autofillOverlayContentService.destroy();
+
+      expect(autofillOverlayContentService["clearUserInteractionEventTimeout"]).toHaveBeenCalled();
+    });
+
+    it("de-registers all global event listeners", () => {
+      jest.spyOn(globalThis.document, "removeEventListener");
+      jest.spyOn(globalThis, "removeEventListener");
+      jest.spyOn(autofillOverlayContentService as any, "removeOverlayRepositionEventListeners");
+
+      autofillOverlayContentService.destroy();
+
+      expect(globalThis.document.removeEventListener).toHaveBeenCalledWith(
+        EVENTS.VISIBILITYCHANGE,
+        autofillOverlayContentService["handleVisibilityChangeEvent"],
+      );
+      expect(globalThis.removeEventListener).toHaveBeenCalledWith(
+        EVENTS.FOCUSOUT,
+        autofillOverlayContentService["handleFormFieldBlurEvent"],
+      );
+      expect(
+        autofillOverlayContentService["removeOverlayRepositionEventListeners"],
+      ).toHaveBeenCalled();
+    });
+
+    it("de-registers any event listeners that are attached to the form field elements", () => {
+      jest.spyOn(autofillOverlayContentService as any, "removeCachedFormFieldEventListeners");
+      jest.spyOn(autofillFieldElement, "removeEventListener");
+      jest.spyOn(autofillOverlayContentService["formFieldElements"], "delete");
+
+      autofillOverlayContentService.destroy();
+
+      expect(
+        autofillOverlayContentService["removeCachedFormFieldEventListeners"],
+      ).toHaveBeenCalledWith(autofillFieldElement);
+      expect(autofillFieldElement.removeEventListener).toHaveBeenCalledWith(
+        EVENTS.BLUR,
+        autofillOverlayContentService["handleFormFieldBlurEvent"],
+      );
+      expect(autofillFieldElement.removeEventListener).toHaveBeenCalledWith(
+        EVENTS.KEYUP,
+        autofillOverlayContentService["handleFormFieldKeyupEvent"],
+      );
+      expect(autofillOverlayContentService["formFieldElements"].delete).toHaveBeenCalledWith(
+        autofillFieldElement,
+      );
+    });
+  });
 });
diff --git a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
index 9e5acae887c..c713c6ea411 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -10,16 +10,12 @@ import AutofillField from "../models/autofill-field";
 import AutofillOverlayButtonIframe from "../overlay/iframe-content/autofill-overlay-button-iframe";
 import AutofillOverlayListIframe from "../overlay/iframe-content/autofill-overlay-list-iframe";
 import { ElementWithOpId, FillableFormFieldElement, FormFieldElement } from "../types";
+import { generateRandomCustomElementName, sendExtensionMessage, setElementStyles } from "../utils";
 import {
   AutofillOverlayElement,
   RedirectFocusDirection,
   AutofillOverlayVisibility,
 } from "../utils/autofill-overlay.enum";
-import {
-  generateRandomCustomElementName,
-  sendExtensionMessage,
-  setElementStyles,
-} from "../utils/utils";
 
 import {
   AutofillOverlayContentService as AutofillOverlayContentServiceInterface,
@@ -32,9 +28,10 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
   isCurrentlyFilling = false;
   isOverlayCiphersPopulated = false;
   pageDetailsUpdateRequired = false;
+  autofillOverlayVisibility: number;
   private readonly findTabs = tabbable;
   private readonly sendExtensionMessage = sendExtensionMessage;
-  private autofillOverlayVisibility: number;
+  private formFieldElements: Set<ElementWithOpId<FormFieldElement>> = new Set([]);
   private userFilledFields: Record<string, FillableFormFieldElement> = {};
   private authStatus: AuthenticationStatus;
   private focusableElements: FocusableElement[] = [];
@@ -47,6 +44,7 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
   private userInteractionEventTimeout: NodeJS.Timeout;
   private overlayElementsMutationObserver: MutationObserver;
   private bodyElementMutationObserver: MutationObserver;
+  private documentElementMutationObserver: MutationObserver;
   private mutationObserverIterations = 0;
   private mutationObserverIterationsResetTimeout: NodeJS.Timeout;
   private autofillFieldKeywordsMap: WeakMap<AutofillField, string> = new WeakMap();
@@ -86,6 +84,8 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
       return;
     }
 
+    this.formFieldElements.add(formFieldElement);
+
     if (!this.autofillOverlayVisibility) {
       await this.getAutofillOverlayVisibility();
     }
@@ -901,10 +901,10 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
       this.handleBodyElementMutationObserverUpdate,
     );
 
-    const documentElementMutationObserver = new MutationObserver(
+    this.documentElementMutationObserver = new MutationObserver(
       this.handleDocumentElementMutationObserverUpdate,
     );
-    documentElementMutationObserver.observe(globalThis.document.documentElement, {
+    this.documentElementMutationObserver.observe(globalThis.document.documentElement, {
       childList: true,
     });
   };
@@ -1117,6 +1117,28 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
     const documentRoot = element.getRootNode() as ShadowRoot | Document;
     return documentRoot?.activeElement;
   }
+
+  /**
+   * Destroys the autofill overlay content service. This method will
+   * disconnect the mutation observers and remove all event listeners.
+   */
+  destroy() {
+    this.documentElementMutationObserver?.disconnect();
+    this.clearUserInteractionEventTimeout();
+    this.formFieldElements.forEach((formFieldElement) => {
+      this.removeCachedFormFieldEventListeners(formFieldElement);
+      formFieldElement.removeEventListener(EVENTS.BLUR, this.handleFormFieldBlurEvent);
+      formFieldElement.removeEventListener(EVENTS.KEYUP, this.handleFormFieldKeyupEvent);
+      this.formFieldElements.delete(formFieldElement);
+    });
+    globalThis.document.removeEventListener(
+      EVENTS.VISIBILITYCHANGE,
+      this.handleVisibilityChangeEvent,
+    );
+    globalThis.removeEventListener(EVENTS.FOCUSOUT, this.handleFormFieldBlurEvent);
+    this.removeAutofillOverlay();
+    this.removeOverlayRepositionEventListeners();
+  }
 }
 
 export default AutofillOverlayContentService;
diff --git a/apps/browser/src/autofill/services/autofill.service.spec.ts b/apps/browser/src/autofill/services/autofill.service.spec.ts
index aa9232c791f..5f9c1db68c3 100644
--- a/apps/browser/src/autofill/services/autofill.service.spec.ts
+++ b/apps/browser/src/autofill/services/autofill.service.spec.ts
@@ -2,7 +2,9 @@ import { mock, mockReset } from "jest-mock-extended";
 
 import { UserVerificationService } from "@bitwarden/common/auth/services/user-verification/user-verification.service";
 import { EventType } from "@bitwarden/common/enums";
+import { FeatureFlag } from "@bitwarden/common/enums/feature-flag.enum";
 import { LogService } from "@bitwarden/common/platform/abstractions/log.service";
+import { ConfigService } from "@bitwarden/common/platform/services/config/config.service";
 import { EventCollectionService } from "@bitwarden/common/services/event/event-collection.service";
 import { SettingsService } from "@bitwarden/common/services/settings.service";
 import {
@@ -24,6 +26,7 @@ import { TotpService } from "@bitwarden/common/vault/services/totp.service";
 
 import { BrowserApi } from "../../platform/browser/browser-api";
 import { BrowserStateService } from "../../platform/services/browser-state.service";
+import { AutofillPort } from "../enums/autofill-port.enums";
 import {
   createAutofillFieldMock,
   createAutofillPageDetailsMock,
@@ -54,6 +57,7 @@ describe("AutofillService", () => {
   const logService = mock<LogService>();
   const settingsService = mock<SettingsService>();
   const userVerificationService = mock<UserVerificationService>();
+  const configService = mock<ConfigService>();
 
   beforeEach(() => {
     autofillService = new AutofillService(
@@ -64,6 +68,7 @@ describe("AutofillService", () => {
       logService,
       settingsService,
       userVerificationService,
+      configService,
     );
   });
 
@@ -72,6 +77,72 @@ describe("AutofillService", () => {
     mockReset(cipherService);
   });
 
+  describe("loadAutofillScriptsOnInstall", () => {
+    let tab1: chrome.tabs.Tab;
+    let tab2: chrome.tabs.Tab;
+    let tab3: chrome.tabs.Tab;
+
+    beforeEach(() => {
+      tab1 = createChromeTabMock({ id: 1, url: "https://some-url.com" });
+      tab2 = createChromeTabMock({ id: 2, url: "http://some-url.com" });
+      tab3 = createChromeTabMock({ id: 3, url: "chrome-extension://some-extension-route" });
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValueOnce([tab1, tab2]);
+    });
+
+    it("queries all browser tabs and injects the autofill scripts into them", async () => {
+      jest.spyOn(autofillService, "injectAutofillScripts");
+
+      await autofillService.loadAutofillScriptsOnInstall();
+
+      expect(BrowserApi.tabsQuery).toHaveBeenCalledWith({});
+      expect(autofillService.injectAutofillScripts).toHaveBeenCalledWith(tab1, 0, false);
+      expect(autofillService.injectAutofillScripts).toHaveBeenCalledWith(tab2, 0, false);
+    });
+
+    it("skips injecting scripts into tabs that do not have an http(s) protocol", async () => {
+      jest.spyOn(autofillService, "injectAutofillScripts");
+
+      await autofillService.loadAutofillScriptsOnInstall();
+
+      expect(BrowserApi.tabsQuery).toHaveBeenCalledWith({});
+      expect(autofillService.injectAutofillScripts).not.toHaveBeenCalledWith(tab3);
+    });
+
+    it("sets up an extension runtime onConnect listener", async () => {
+      await autofillService.loadAutofillScriptsOnInstall();
+
+      // eslint-disable-next-line no-restricted-syntax
+      expect(chrome.runtime.onConnect.addListener).toHaveBeenCalledWith(expect.any(Function));
+    });
+  });
+
+  describe("reloadAutofillScripts", () => {
+    it("disconnects and removes all autofill script ports", () => {
+      const port1 = mock<chrome.runtime.Port>({
+        disconnect: jest.fn(),
+      });
+      const port2 = mock<chrome.runtime.Port>({
+        disconnect: jest.fn(),
+      });
+      autofillService["autofillScriptPortsSet"] = new Set([port1, port2]);
+
+      autofillService.reloadAutofillScripts();
+
+      expect(port1.disconnect).toHaveBeenCalled();
+      expect(port2.disconnect).toHaveBeenCalled();
+      expect(autofillService["autofillScriptPortsSet"].size).toBe(0);
+    });
+
+    it("re-injects the autofill scripts in all tabs", () => {
+      autofillService["autofillScriptPortsSet"] = new Set([mock<chrome.runtime.Port>()]);
+      jest.spyOn(autofillService as any, "injectAutofillScriptsInAllTabs");
+
+      autofillService.reloadAutofillScripts();
+
+      expect(autofillService["injectAutofillScriptsInAllTabs"]).toHaveBeenCalled();
+    });
+  });
+
   describe("injectAutofillScripts", () => {
     const autofillV1Script = "autofill.js";
     const autofillV2BootstrapScript = "bootstrap-autofill.js";
@@ -83,12 +154,12 @@ describe("AutofillService", () => {
 
     beforeEach(() => {
       tabMock = createChromeTabMock();
-      sender = { tab: tabMock };
+      sender = { tab: tabMock, frameId: 1 };
       jest.spyOn(BrowserApi, "executeScriptInTab").mockImplementation();
     });
 
     it("accepts an extension message sender and injects the autofill scripts into the tab of the sender", async () => {
-      await autofillService.injectAutofillScripts(sender);
+      await autofillService.injectAutofillScripts(sender.tab, sender.frameId, true);
 
       [autofillV1Script, ...defaultAutofillScripts].forEach((scriptName) => {
         expect(BrowserApi.executeScriptInTab).toHaveBeenCalledWith(tabMock.id, {
@@ -105,7 +176,11 @@ describe("AutofillService", () => {
     });
 
     it("will inject the bootstrap-autofill script if the enableAutofillV2 flag is set", async () => {
-      await autofillService.injectAutofillScripts(sender, true);
+      jest
+        .spyOn(configService, "getFeatureFlag")
+        .mockImplementation((flag) => Promise.resolve(flag === FeatureFlag.AutofillV2));
+
+      await autofillService.injectAutofillScripts(sender.tab, sender.frameId);
 
       expect(BrowserApi.executeScriptInTab).toHaveBeenCalledWith(tabMock.id, {
         file: `content/${autofillV2BootstrapScript}`,
@@ -120,11 +195,16 @@ describe("AutofillService", () => {
     });
 
     it("will inject the bootstrap-autofill-overlay script if the enableAutofillOverlay flag is set and the user has the autofill overlay enabled", async () => {
+      jest
+        .spyOn(configService, "getFeatureFlag")
+        .mockImplementation((flag) =>
+          Promise.resolve(flag === FeatureFlag.AutofillOverlay || flag === FeatureFlag.AutofillV2),
+        );
       jest
         .spyOn(autofillService["settingsService"], "getAutoFillOverlayVisibility")
         .mockResolvedValue(AutofillOverlayVisibility.OnFieldFocus);
 
-      await autofillService.injectAutofillScripts(sender, true, true);
+      await autofillService.injectAutofillScripts(sender.tab, sender.frameId);
 
       expect(BrowserApi.executeScriptInTab).toHaveBeenCalledWith(tabMock.id, {
         file: `content/${autofillOverlayBootstrapScript}`,
@@ -144,18 +224,25 @@ describe("AutofillService", () => {
     });
 
     it("will inject the bootstrap-autofill script if the enableAutofillOverlay flag is set but the user does not have the autofill overlay enabled", async () => {
+      jest
+        .spyOn(configService, "getFeatureFlag")
+        .mockImplementation((flag) =>
+          Promise.resolve(flag === FeatureFlag.AutofillOverlay || flag === FeatureFlag.AutofillV2),
+        );
       jest
         .spyOn(autofillService["settingsService"], "getAutoFillOverlayVisibility")
         .mockResolvedValue(AutofillOverlayVisibility.Off);
 
-      await autofillService.injectAutofillScripts(sender, true, true);
+      await autofillService.injectAutofillScripts(sender.tab, sender.frameId);
 
       expect(BrowserApi.executeScriptInTab).toHaveBeenCalledWith(tabMock.id, {
         file: `content/${autofillV2BootstrapScript}`,
+        frameId: sender.frameId,
         ...defaultExecuteScriptOptions,
       });
       expect(BrowserApi.executeScriptInTab).not.toHaveBeenCalledWith(tabMock.id, {
         file: `content/${autofillV1Script}`,
+        frameId: sender.frameId,
         ...defaultExecuteScriptOptions,
       });
     });
@@ -4436,4 +4523,58 @@ describe("AutofillService", () => {
       expect(autofillService["currentlyOpeningPasswordRepromptPopout"]).toBe(false);
     });
   });
+
+  describe("handleInjectedScriptPortConnection", () => {
+    it("ignores port connections that do not have the correct port name", () => {
+      const port = mock<chrome.runtime.Port>({
+        name: "some-invalid-port-name",
+        onDisconnect: { addListener: jest.fn() },
+      }) as any;
+
+      autofillService["handleInjectedScriptPortConnection"](port);
+
+      expect(port.onDisconnect.addListener).not.toHaveBeenCalled();
+      expect(autofillService["autofillScriptPortsSet"].size).toBe(0);
+    });
+
+    it("adds the connect port to the set of injected script ports and sets up an onDisconnect listener", () => {
+      const port = mock<chrome.runtime.Port>({
+        name: AutofillPort.InjectedScript,
+        onDisconnect: { addListener: jest.fn() },
+      }) as any;
+      jest.spyOn(autofillService as any, "handleInjectScriptPortOnDisconnect");
+
+      autofillService["handleInjectedScriptPortConnection"](port);
+
+      expect(port.onDisconnect.addListener).toHaveBeenCalledWith(
+        autofillService["handleInjectScriptPortOnDisconnect"],
+      );
+      expect(autofillService["autofillScriptPortsSet"].size).toBe(1);
+    });
+  });
+
+  describe("handleInjectScriptPortOnDisconnect", () => {
+    it("ignores port disconnections that do not have the correct port name", () => {
+      autofillService["autofillScriptPortsSet"].add(mock<chrome.runtime.Port>());
+
+      autofillService["handleInjectScriptPortOnDisconnect"](
+        mock<chrome.runtime.Port>({
+          name: "some-invalid-port-name",
+        }),
+      );
+
+      expect(autofillService["autofillScriptPortsSet"].size).toBe(1);
+    });
+
+    it("removes the port from the set of injected script ports", () => {
+      const port = mock<chrome.runtime.Port>({
+        name: AutofillPort.InjectedScript,
+      }) as any;
+      autofillService["autofillScriptPortsSet"].add(port);
+
+      autofillService["handleInjectScriptPortOnDisconnect"](port);
+
+      expect(autofillService["autofillScriptPortsSet"].size).toBe(0);
+    });
+  });
 });
diff --git a/apps/browser/src/autofill/services/autofill.service.ts b/apps/browser/src/autofill/services/autofill.service.ts
index a1ef5a47a1c..eddc8f93a9e 100644
--- a/apps/browser/src/autofill/services/autofill.service.ts
+++ b/apps/browser/src/autofill/services/autofill.service.ts
@@ -2,6 +2,8 @@ import { EventCollectionService } from "@bitwarden/common/abstractions/event/eve
 import { SettingsService } from "@bitwarden/common/abstractions/settings.service";
 import { UserVerificationService } from "@bitwarden/common/auth/abstractions/user-verification/user-verification.service.abstraction";
 import { EventType } from "@bitwarden/common/enums";
+import { FeatureFlag } from "@bitwarden/common/enums/feature-flag.enum";
+import { ConfigServiceAbstraction } from "@bitwarden/common/platform/abstractions/config/config.service.abstraction";
 import { LogService } from "@bitwarden/common/platform/abstractions/log.service";
 import { CipherService } from "@bitwarden/common/vault/abstractions/cipher.service";
 import { TotpService } from "@bitwarden/common/vault/abstractions/totp.service";
@@ -13,6 +15,7 @@ import { FieldView } from "@bitwarden/common/vault/models/view/field.view";
 import { BrowserApi } from "../../platform/browser/browser-api";
 import { BrowserStateService } from "../../platform/services/abstractions/browser-state.service";
 import { openVaultItemPasswordRepromptPopout } from "../../vault/popup/utils/vault-popout-window";
+import { AutofillPort } from "../enums/autofill-port.enums";
 import AutofillField from "../models/autofill-field";
 import AutofillPageDetails from "../models/autofill-page-details";
 import AutofillScript from "../models/autofill-script";
@@ -35,6 +38,7 @@ export default class AutofillService implements AutofillServiceInterface {
   private openVaultItemPasswordRepromptPopout = openVaultItemPasswordRepromptPopout;
   private openPasswordRepromptPopoutDebounce: NodeJS.Timeout;
   private currentlyOpeningPasswordRepromptPopout = false;
+  private autofillScriptPortsSet = new Set<chrome.runtime.Port>();
 
   constructor(
     private cipherService: CipherService,
@@ -44,23 +48,54 @@ export default class AutofillService implements AutofillServiceInterface {
     private logService: LogService,
     private settingsService: SettingsService,
     private userVerificationService: UserVerificationService,
+    private configService: ConfigServiceAbstraction,
   ) {}
 
+  /**
+   * Triggers on installation of the extension Handles injecting
+   * content scripts into all tabs that are currently open, and
+   * sets up a listener to ensure content scripts can identify
+   * if the extension context has been disconnected.
+   */
+  async loadAutofillScriptsOnInstall() {
+    BrowserApi.addListener(chrome.runtime.onConnect, this.handleInjectedScriptPortConnection);
+
+    this.injectAutofillScriptsInAllTabs();
+  }
+
+  /**
+   * Triggers a complete reload of all autofill scripts on tabs open within
+   * the user's browsing session. This is done by first disconnecting all
+   * existing autofill content script ports, which cleans up existing object
+   * instances, and then re-injecting the autofill scripts into all tabs.
+   */
+  async reloadAutofillScripts() {
+    this.autofillScriptPortsSet.forEach((port) => {
+      port.disconnect();
+      this.autofillScriptPortsSet.delete(port);
+    });
+
+    this.injectAutofillScriptsInAllTabs();
+  }
+
   /**
    * Injects the autofill scripts into the current tab and all frames
    * found within the tab. Temporarily, will conditionally inject
    * the refactor of the core autofill script if the feature flag
    * is enabled.
-   * @param {chrome.runtime.MessageSender} sender
-   * @param {boolean} autofillV2
-   * @param {boolean} autofillOverlay
-   * @returns {Promise<void>}
+   * @param {chrome.tabs.Tab} tab
+   * @param {number} frameId
+   * @param {boolean} triggeringOnPageLoad
    */
   async injectAutofillScripts(
-    sender: chrome.runtime.MessageSender,
-    autofillV2 = false,
-    autofillOverlay = false,
-  ) {
+    tab: chrome.tabs.Tab,
+    frameId = 0,
+    triggeringOnPageLoad = true,
+  ): Promise<void> {
+    const autofillV2 = await this.configService.getFeatureFlag<boolean>(FeatureFlag.AutofillV2);
+    const autofillOverlay = await this.configService.getFeatureFlag<boolean>(
+      FeatureFlag.AutofillOverlay,
+    );
     let mainAutofillScript = "autofill.js";
 
     const isUsingAutofillOverlay =
@@ -73,20 +108,24 @@ export default class AutofillService implements AutofillServiceInterface {
         : "bootstrap-autofill.js";
     }
 
-    const injectedScripts = [
-      mainAutofillScript,
-      "autofiller.js",
-      "notificationBar.js",
-      "contextMenuHandler.js",
-    ];
+    const injectedScripts = [mainAutofillScript];
+    if (triggeringOnPageLoad) {
+      injectedScripts.push("autofiller.js");
+    }
+    injectedScripts.push("notificationBar.js", "contextMenuHandler.js");
 
     for (const injectedScript of injectedScripts) {
-      await BrowserApi.executeScriptInTab(sender.tab.id, {
+      await BrowserApi.executeScriptInTab(tab.id, {
         file: `content/${injectedScript}`,
-        frameId: sender.frameId,
+        frameId,
         runAt: "document_start",
       });
     }
+
+    await BrowserApi.executeScriptInTab(tab.id, {
+      file: "content/message_handler.js",
+      runAt: "document_start",
+    });
   }
 
   /**
@@ -1877,4 +1916,47 @@ export default class AutofillService implements AutofillServiceInterface {
 
     return false;
   }
+
+  /**
+   * Handles incoming long-lived connections from injected autofill scripts.
+   * Stores the port in a set to facilitate disconnecting ports if the extension
+   * needs to re-inject the autofill scripts.
+   *
+   * @param port - The port that was connected
+   */
+  private handleInjectedScriptPortConnection = (port: chrome.runtime.Port) => {
+    if (port.name !== AutofillPort.InjectedScript) {
+      return;
+    }
+
+    this.autofillScriptPortsSet.add(port);
+    port.onDisconnect.addListener(this.handleInjectScriptPortOnDisconnect);
+  };
+
+  /**
+   * Handles disconnecting ports that relate to injected autofill scripts.
+
+   * @param port - The port that was disconnected
+   */
+  private handleInjectScriptPortOnDisconnect = (port: chrome.runtime.Port) => {
+    if (port.name !== AutofillPort.InjectedScript) {
+      return;
+    }
+
+    this.autofillScriptPortsSet.delete(port);
+  };
+
+  /**
+   * Queries all open tabs in the user's browsing session
+   * and injects the autofill scripts into the page.
+   */
+  private async injectAutofillScriptsInAllTabs() {
+    const tabs = await BrowserApi.tabsQuery({});
+    for (let index = 0; index < tabs.length; index++) {
+      const tab = tabs[index];
+      if (tab.url?.startsWith("http")) {
+        this.injectAutofillScripts(tab, 0, false);
+      }
+    }
+  }
 }
diff --git a/apps/browser/src/autofill/services/collect-autofill-content.service.ts b/apps/browser/src/autofill/services/collect-autofill-content.service.ts
index d675a37921d..ebddc201417 100644
--- a/apps/browser/src/autofill/services/collect-autofill-content.service.ts
+++ b/apps/browser/src/autofill/services/collect-autofill-content.service.ts
@@ -1249,6 +1249,17 @@ class CollectAutofillContentService implements CollectAutofillContentServiceInte
 
     return attributeValue;
   }
+
+  /**
+   * Destroys the CollectAutofillContentService. Clears all
+   * timeouts and disconnects the mutation observer.
+   */
+  destroy() {
+    if (this.updateAutofillElementsAfterMutationTimeout) {
+      clearTimeout(this.updateAutofillElementsAfterMutationTimeout);
+    }
+    this.mutationObserver?.disconnect();
+  }
 }
 
 export default CollectAutofillContentService;
diff --git a/apps/browser/src/autofill/utils/utils.spec.ts b/apps/browser/src/autofill/utils/index.spec.ts
similarity index 51%
rename from apps/browser/src/autofill/utils/utils.spec.ts
rename to apps/browser/src/autofill/utils/index.spec.ts
index 1da83fef242..4024d5839a8 100644
--- a/apps/browser/src/autofill/utils/utils.spec.ts
+++ b/apps/browser/src/autofill/utils/index.spec.ts
@@ -1,10 +1,17 @@
+import { AutofillPort } from "../enums/autofill-port.enums";
+import { triggerPortOnDisconnectEvent } from "../jest/testing-utils";
+
 import { logoIcon, logoLockedIcon } from "./svg-icons";
+
 import {
   buildSvgDomElement,
   generateRandomCustomElementName,
   sendExtensionMessage,
   setElementStyles,
-} from "./utils";
+  getFromLocalStorage,
+  setupExtensionDisconnectAction,
+  setupAutofillInitDisconnectAction,
+} from "./index";
 
 describe("buildSvgDomElement", () => {
   it("returns an SVG DOM element", () => {
@@ -116,3 +123,107 @@ describe("setElementStyles", () => {
     expect(testDiv.style.cssText).toEqual(expectedCSSRuleString);
   });
 });
+
+describe("getFromLocalStorage", () => {
+  it("returns a promise with the storage object pulled from the extension storage api", async () => {
+    const localStorage: Record<string, any> = {
+      testValue: "test",
+      another: "another",
+    };
+    jest.spyOn(chrome.storage.local, "get").mockImplementation((keys, callback) => {
+      const localStorageObject: Record<string, string> = {};
+
+      if (typeof keys === "string") {
+        localStorageObject[keys] = localStorage[keys];
+      } else if (Array.isArray(keys)) {
+        for (const key of keys) {
+          localStorageObject[key] = localStorage[key];
+        }
+      }
+
+      callback(localStorageObject);
+    });
+
+    const returnValue = await getFromLocalStorage("testValue");
+
+    expect(chrome.storage.local.get).toHaveBeenCalled();
+    expect(returnValue).toEqual({ testValue: "test" });
+  });
+});
+
+describe("setupExtensionDisconnectAction", () => {
+  afterEach(() => {
+    jest.clearAllMocks();
+  });
+
+  it("connects a port to the extension background and sets up an onDisconnect listener", () => {
+    const onDisconnectCallback = jest.fn();
+    let port: chrome.runtime.Port;
+    jest.spyOn(chrome.runtime, "connect").mockImplementation(() => {
+      port = {
+        onDisconnect: {
+          addListener: onDisconnectCallback,
+          removeListener: jest.fn(),
+        },
+      } as unknown as chrome.runtime.Port;
+
+      return port;
+    });
+
+    setupExtensionDisconnectAction(onDisconnectCallback);
+
+    expect(chrome.runtime.connect).toHaveBeenCalledWith({
+      name: AutofillPort.InjectedScript,
+    });
+    expect(port.onDisconnect.addListener).toHaveBeenCalledWith(expect.any(Function));
+  });
+});
+
+describe("setupAutofillInitDisconnectAction", () => {
+  afterEach(() => {
+    jest.clearAllMocks();
+  });
+
+  it("skips setting up the extension disconnect action if the bitwardenAutofillInit object is not populated", () => {
+    const onDisconnectCallback = jest.fn();
+    window.bitwardenAutofillInit = undefined;
+    const portConnectSpy = jest.spyOn(chrome.runtime, "connect").mockImplementation(() => {
+      return {
+        onDisconnect: {
+          addListener: onDisconnectCallback,
+          removeListener: jest.fn(),
+        },
+      } as unknown as chrome.runtime.Port;
+    });
+
+    setupAutofillInitDisconnectAction(window);
+
+    expect(portConnectSpy).not.toHaveBeenCalled();
+  });
+
+  it("destroys the autofill init instance when the port is disconnected", () => {
+    let port: chrome.runtime.Port;
+    const autofillInitDestroy: CallableFunction = jest.fn();
+    window.bitwardenAutofillInit = {
+      destroy: autofillInitDestroy,
+    } as any;
+    jest.spyOn(chrome.runtime, "connect").mockImplementation(() => {
+      port = {
+        onDisconnect: {
+          addListener: jest.fn(),
+          removeListener: jest.fn(),
+        },
+      } as unknown as chrome.runtime.Port;
+
+      return port;
+    });
+
+    setupAutofillInitDisconnectAction(window);
+    triggerPortOnDisconnectEvent(port as chrome.runtime.Port);
+
+    expect(chrome.runtime.connect).toHaveBeenCalled();
+    expect(port.onDisconnect.addListener).toHaveBeenCalled();
+    expect(autofillInitDestroy).toHaveBeenCalled();
+    expect(window.bitwardenAutofillInit).toBeUndefined();
+  });
+});
diff --git a/apps/browser/src/autofill/utils/utils.ts b/apps/browser/src/autofill/utils/index.ts
similarity index 65%
rename from apps/browser/src/autofill/utils/utils.ts
rename to apps/browser/src/autofill/utils/index.ts
index 73e133da32c..a2ce51c8cc1 100644
--- a/apps/browser/src/autofill/utils/utils.ts
+++ b/apps/browser/src/autofill/utils/index.ts
@@ -1,3 +1,5 @@
+import { AutofillPort } from "../enums/autofill-port.enums";
+
 /**
  * Generates a random string of characters that formatted as a custom element name.
  */
@@ -103,9 +105,57 @@ function setElementStyles(
   }
 }
 
+/**
+ * Get data from local storage based on the keys provided.
+ *
+ * @param keys - String or array of strings of keys to get from local storage
+ */
+async function getFromLocalStorage(keys: string | string[]): Promise<Record<string, any>> {
+  return new Promise((resolve) => {
+    chrome.storage.local.get(keys, (storage: Record<string, any>) => resolve(storage));
+  });
+}
+
+/**
+ * Sets up a long-lived connection with the extension background
+ * and triggers an onDisconnect event if the extension context
+ * is invalidated.
+ *
+ * @param callback - Callback function to run when the extension disconnects
+ */
+function setupExtensionDisconnectAction(callback: (port: chrome.runtime.Port) => void) {
+  const port = chrome.runtime.connect({ name: AutofillPort.InjectedScript });
+  const onDisconnectCallback = (disconnectedPort: chrome.runtime.Port) => {
+    callback(disconnectedPort);
+    port.onDisconnect.removeListener(onDisconnectCallback);
+  };
+  port.onDisconnect.addListener(onDisconnectCallback);
+}
+
+/**
+ * Handles setup of the extension disconnect action for the autofill init class
+ * in both instances where the overlay might or might not be initialized.
+ *
+ * @param windowContext - The global window context
+ */
+function setupAutofillInitDisconnectAction(windowContext: Window) {
+  if (!windowContext.bitwardenAutofillInit) {
+    return;
+  }
+
+  const onDisconnectCallback = () => {
+    windowContext.bitwardenAutofillInit.destroy();
+    delete windowContext.bitwardenAutofillInit;
+  };
+  setupExtensionDisconnectAction(onDisconnectCallback);
+}
+
 export {
   generateRandomCustomElementName,
   buildSvgDomElement,
   sendExtensionMessage,
   setElementStyles,
+  getFromLocalStorage,
+  setupExtensionDisconnectAction,
+  setupAutofillInitDisconnectAction,
 };
diff --git a/apps/browser/src/background/idle.background.ts b/apps/browser/src/background/idle.background.ts
index ccc76883b11..7ef6f7090bd 100644
--- a/apps/browser/src/background/idle.background.ts
+++ b/apps/browser/src/background/idle.background.ts
@@ -1,5 +1,8 @@
+import { firstValueFrom } from "rxjs";
+
 import { NotificationsService } from "@bitwarden/common/abstractions/notifications.service";
 import { VaultTimeoutService } from "@bitwarden/common/abstractions/vault-timeout/vault-timeout.service";
+import { AccountService } from "@bitwarden/common/auth/abstractions/account.service";
 import { VaultTimeoutAction } from "@bitwarden/common/enums/vault-timeout-action.enum";
 
 import { BrowserStateService } from "../platform/services/abstractions/browser-state.service";
@@ -7,7 +10,7 @@ import { BrowserStateService } from "../platform/services/abstractions/browser-s
 const IdleInterval = 60 * 5; // 5 minutes
 
 export default class IdleBackground {
-  private idle: any;
+  private idle: typeof chrome.idle | typeof browser.idle | null;
   private idleTimer: number = null;
   private idleState = "active";
 
@@ -15,6 +18,7 @@ export default class IdleBackground {
     private vaultTimeoutService: VaultTimeoutService,
     private stateService: BrowserStateService,
     private notificationsService: NotificationsService,
+    private accountService: AccountService,
   ) {
     this.idle = chrome.idle || (browser != null ? browser.idle : null);
   }
@@ -39,21 +43,27 @@ export default class IdleBackground {
     }
 
     if (this.idle.onStateChanged) {
-      this.idle.onStateChanged.addListener(async (newState: string) => {
-        if (newState === "locked") {
-          // If the screen is locked or the screensaver activates
-          const timeout = await this.stateService.getVaultTimeout();
-          if (timeout === -2) {
-            // On System Lock vault timeout option
-            const action = await this.stateService.getVaultTimeoutAction();
-            if (action === VaultTimeoutAction.LogOut) {
-              await this.vaultTimeoutService.logOut();
-            } else {
-              await this.vaultTimeoutService.lock();
+      this.idle.onStateChanged.addListener(
+        async (newState: chrome.idle.IdleState | browser.idle.IdleState) => {
+          if (newState === "locked") {
+            // Need to check if any of the current users have their timeout set to `onLocked`
+            const allUsers = await firstValueFrom(this.accountService.accounts$);
+            for (const userId in allUsers) {
+              // If the screen is locked or the screensaver activates
+              const timeout = await this.stateService.getVaultTimeout({ userId: userId });
+              if (timeout === -2) {
+                // On System Lock vault timeout option
+                const action = await this.stateService.getVaultTimeoutAction({ userId: userId });
+                if (action === VaultTimeoutAction.LogOut) {
+                  await this.vaultTimeoutService.logOut(userId);
+                } else {
+                  await this.vaultTimeoutService.lock(userId);
+                }
+              }
             }
           }
-        }
-      });
+        },
+      );
     }
   }
 
diff --git a/apps/browser/src/background/main.background.ts b/apps/browser/src/background/main.background.ts
index 2c1573d4e9b..fa77c498953 100644
--- a/apps/browser/src/background/main.background.ts
+++ b/apps/browser/src/background/main.background.ts
@@ -566,6 +566,7 @@ export default class MainBackground {
       this.logService,
       this.settingsService,
       this.userVerificationService,
+      this.configService,
     );
     this.auditService = new AuditService(this.cryptoFunctionService, this.apiService);
 
@@ -729,6 +730,7 @@ export default class MainBackground {
       this.vaultTimeoutService,
       this.stateService,
       this.notificationsService,
+      this.accountService,
     );
     this.webRequestBackground = new WebRequestBackground(
       this.platformUtilsService,
diff --git a/apps/browser/src/background/runtime.background.ts b/apps/browser/src/background/runtime.background.ts
index fcaefc7c5e2..de43e585603 100644
--- a/apps/browser/src/background/runtime.background.ts
+++ b/apps/browser/src/background/runtime.background.ts
@@ -1,5 +1,4 @@
 import { NotificationsService } from "@bitwarden/common/abstractions/notifications.service";
-import { FeatureFlag } from "@bitwarden/common/enums/feature-flag.enum";
 import { ConfigServiceAbstraction } from "@bitwarden/common/platform/abstractions/config/config.service.abstraction";
 import { I18nService } from "@bitwarden/common/platform/abstractions/i18n.service";
 import { LogService } from "@bitwarden/common/platform/abstractions/log.service";
@@ -97,9 +96,9 @@ export default class RuntimeBackground {
           await closeUnlockPopout();
         }
 
+        await this.notificationsService.updateConnection(msg.command === "loggedIn");
         await this.main.refreshBadge();
         await this.main.refreshMenu(false);
-        this.notificationsService.updateConnection(msg.command === "unlocked");
         this.systemService.cancelProcessReload();
 
         if (item) {
@@ -133,11 +132,7 @@ export default class RuntimeBackground {
         await this.main.openPopup();
         break;
       case "triggerAutofillScriptInjection":
-        await this.autofillService.injectAutofillScripts(
-          sender,
-          await this.configService.getFeatureFlag<boolean>(FeatureFlag.AutofillV2),
-          await this.configService.getFeatureFlag<boolean>(FeatureFlag.AutofillOverlay),
-        );
+        await this.autofillService.injectAutofillScripts(sender.tab, sender.frameId);
         break;
       case "bgCollectPageDetails":
         await this.main.collectPageDetailsForContentScript(sender.tab, msg.sender, sender.frameId);
@@ -325,6 +320,8 @@ export default class RuntimeBackground {
 
   private async checkOnInstalled() {
     setTimeout(async () => {
+      this.autofillService.loadAutofillScriptsOnInstall();
+
       if (this.onInstalledReason != null) {
         if (this.onInstalledReason === "install") {
           BrowserApi.createNewTab("https://bitwarden.com/browser-start/");
diff --git a/apps/browser/src/manifest.json b/apps/browser/src/manifest.json
index aa71d648e8e..09f12c56f18 100644
--- a/apps/browser/src/manifest.json
+++ b/apps/browser/src/manifest.json
@@ -24,12 +24,6 @@
       "matches": ["http://*/*", "https://*/*", "file:///*"],
       "run_at": "document_start"
     },
-    {
-      "all_frames": false,
-      "js": ["content/message_handler.js"],
-      "matches": ["http://*/*", "https://*/*", "file:///*"],
-      "run_at": "document_start"
-    },
     {
       "all_frames": true,
       "css": ["content/autofill.css"],
diff --git a/apps/browser/test.setup.ts b/apps/browser/test.setup.ts
index 2da36f0a5a5..647e4cfdfb3 100644
--- a/apps/browser/test.setup.ts
+++ b/apps/browser/test.setup.ts
@@ -23,11 +23,12 @@ const runtime = {
     removeListener: jest.fn(),
   },
   sendMessage: jest.fn(),
-  getManifest: jest.fn(),
+  getManifest: jest.fn(() => ({ version: 2 })),
   getURL: jest.fn((path) => `chrome-extension://id/${path}`),
   connect: jest.fn(),
   onConnect: {
     addListener: jest.fn(),
+    removeListener: jest.fn(),
   },
 };
 
diff --git a/apps/desktop/src/auth/lock.component.spec.ts b/apps/desktop/src/auth/lock.component.spec.ts
new file mode 100644
index 00000000000..fa947319571
--- /dev/null
+++ b/apps/desktop/src/auth/lock.component.spec.ts
@@ -0,0 +1,394 @@
+import { NO_ERRORS_SCHEMA } from "@angular/core";
+import { ComponentFixture, TestBed, fakeAsync, tick } from "@angular/core/testing";
+import { ActivatedRoute } from "@angular/router";
+import { MockProxy, mock } from "jest-mock-extended";
+import { of } from "rxjs";
+
+import { LockComponent as BaseLockComponent } from "@bitwarden/angular/auth/components/lock.component";
+import { I18nPipe } from "@bitwarden/angular/platform/pipes/i18n.pipe";
+import { ApiService } from "@bitwarden/common/abstractions/api.service";
+import { VaultTimeoutSettingsService } from "@bitwarden/common/abstractions/vault-timeout/vault-timeout-settings.service";
+import { VaultTimeoutService } from "@bitwarden/common/abstractions/vault-timeout/vault-timeout.service";
+import { PolicyApiServiceAbstraction } from "@bitwarden/common/admin-console/abstractions/policy/policy-api.service.abstraction";
+import { InternalPolicyService } from "@bitwarden/common/admin-console/abstractions/policy/policy.service.abstraction";
+import { DeviceTrustCryptoServiceAbstraction } from "@bitwarden/common/auth/abstractions/device-trust-crypto.service.abstraction";
+import { UserVerificationService } from "@bitwarden/common/auth/abstractions/user-verification/user-verification.service.abstraction";
+import { BroadcasterService } from "@bitwarden/common/platform/abstractions/broadcaster.service";
+import { CryptoService } from "@bitwarden/common/platform/abstractions/crypto.service";
+import { EnvironmentService } from "@bitwarden/common/platform/abstractions/environment.service";
+import { I18nService } from "@bitwarden/common/platform/abstractions/i18n.service";
+import { LogService } from "@bitwarden/common/platform/abstractions/log.service";
+import { MessagingService } from "@bitwarden/common/platform/abstractions/messaging.service";
+import { PlatformUtilsService } from "@bitwarden/common/platform/abstractions/platform-utils.service";
+import { PasswordStrengthServiceAbstraction } from "@bitwarden/common/tools/password-strength";
+import { DialogService } from "@bitwarden/components";
+
+import { ElectronStateService } from "../platform/services/electron-state.service.abstraction";
+
+import { LockComponent } from "./lock.component";
+
+// ipc mock global
+const isWindowVisibleMock = jest.fn();
+(global as any).ipc = {
+  platform: {
+    biometric: {
+      enabled: jest.fn(),
+    },
+    isWindowVisible: isWindowVisibleMock,
+  },
+};
+
+describe("LockComponent", () => {
+  let component: LockComponent;
+  let fixture: ComponentFixture<LockComponent>;
+  let stateServiceMock: MockProxy<ElectronStateService>;
+  let messagingServiceMock: MockProxy<MessagingService>;
+  let broadcasterServiceMock: MockProxy<BroadcasterService>;
+  let platformUtilsServiceMock: MockProxy<PlatformUtilsService>;
+  let activatedRouteMock: MockProxy<ActivatedRoute>;
+
+  beforeEach(() => {
+    stateServiceMock = mock<ElectronStateService>();
+    stateServiceMock.activeAccount$ = of(null);
+
+    messagingServiceMock = mock<MessagingService>();
+    broadcasterServiceMock = mock<BroadcasterService>();
+    platformUtilsServiceMock = mock<PlatformUtilsService>();
+
+    activatedRouteMock = mock<ActivatedRoute>();
+    activatedRouteMock.queryParams = mock<ActivatedRoute["queryParams"]>();
+
+    TestBed.configureTestingModule({
+      declarations: [LockComponent, I18nPipe],
+      providers: [
+        {
+          provide: I18nService,
+          useValue: mock<I18nService>(),
+        },
+        {
+          provide: PlatformUtilsService,
+          useValue: platformUtilsServiceMock,
+        },
+        {
+          provide: MessagingService,
+          useValue: messagingServiceMock,
+        },
+        {
+          provide: CryptoService,
+          useValue: mock<CryptoService>(),
+        },
+        {
+          provide: VaultTimeoutService,
+          useValue: mock<VaultTimeoutService>(),
+        },
+        {
+          provide: VaultTimeoutSettingsService,
+          useValue: mock<VaultTimeoutSettingsService>(),
+        },
+        {
+          provide: EnvironmentService,
+          useValue: mock<EnvironmentService>(),
+        },
+        {
+          provide: ElectronStateService,
+          useValue: stateServiceMock,
+        },
+        {
+          provide: ApiService,
+          useValue: mock<ApiService>(),
+        },
+        {
+          provide: ActivatedRoute,
+          useValue: activatedRouteMock,
+        },
+        {
+          provide: BroadcasterService,
+          useValue: broadcasterServiceMock,
+        },
+        {
+          provide: PolicyApiServiceAbstraction,
+          useValue: mock<PolicyApiServiceAbstraction>(),
+        },
+        {
+          provide: InternalPolicyService,
+          useValue: mock<InternalPolicyService>(),
+        },
+        {
+          provide: PasswordStrengthServiceAbstraction,
+          useValue: mock<PasswordStrengthServiceAbstraction>(),
+        },
+        {
+          provide: LogService,
+          useValue: mock<LogService>(),
+        },
+        {
+          provide: DialogService,
+          useValue: mock<DialogService>(),
+        },
+        {
+          provide: DeviceTrustCryptoServiceAbstraction,
+          useValue: mock<DeviceTrustCryptoServiceAbstraction>(),
+        },
+        {
+          provide: UserVerificationService,
+          useValue: mock<UserVerificationService>(),
+        },
+      ],
+      schemas: [NO_ERRORS_SCHEMA],
+    }).compileComponents();
+  });
+
+  beforeEach(() => {
+    fixture = TestBed.createComponent(LockComponent);
+    component = fixture.componentInstance;
+    fixture.detectChanges();
+    jest.clearAllMocks();
+  });
+
+  describe("ngOnInit", () => {
+    it("should call super.ngOnInit() once", async () => {
+      const superNgOnInitSpy = jest.spyOn(BaseLockComponent.prototype, "ngOnInit");
+      await component.ngOnInit();
+      expect(superNgOnInitSpy).toHaveBeenCalledTimes(1);
+    });
+
+    it('should set "autoPromptBiometric" to true if "stateService.getDisableAutoBiometricsPrompt()" resolves to false', async () => {
+      stateServiceMock.getDisableAutoBiometricsPrompt.mockResolvedValue(false);
+
+      await component.ngOnInit();
+      expect(component["autoPromptBiometric"]).toBe(true);
+    });
+
+    it('should set "autoPromptBiometric" to false if "stateService.getDisableAutoBiometricsPrompt()" resolves to true', async () => {
+      stateServiceMock.getDisableAutoBiometricsPrompt.mockResolvedValue(true);
+
+      await component.ngOnInit();
+      expect(component["autoPromptBiometric"]).toBe(false);
+    });
+
+    it('should set "biometricReady" to true if "stateService.getBiometricReady()" resolves to true', async () => {
+      component["canUseBiometric"] = jest.fn().mockResolvedValue(true);
+
+      await component.ngOnInit();
+      expect(component["biometricReady"]).toBe(true);
+    });
+
+    it('should set "biometricReady" to false if "stateService.getBiometricReady()" resolves to false', async () => {
+      component["canUseBiometric"] = jest.fn().mockResolvedValue(false);
+
+      await component.ngOnInit();
+      expect(component["biometricReady"]).toBe(false);
+    });
+
+    it("should call displayBiometricUpdateWarning", async () => {
+      component["displayBiometricUpdateWarning"] = jest.fn();
+      await component.ngOnInit();
+      expect(component["displayBiometricUpdateWarning"]).toHaveBeenCalledTimes(1);
+    });
+
+    it("should call delayedAskForBiometric", async () => {
+      component["delayedAskForBiometric"] = jest.fn();
+      await component.ngOnInit();
+      expect(component["delayedAskForBiometric"]).toHaveBeenCalledTimes(1);
+      expect(component["delayedAskForBiometric"]).toHaveBeenCalledWith(500);
+    });
+
+    it("should call delayedAskForBiometric when queryParams change", async () => {
+      activatedRouteMock.queryParams = of({ promptBiometric: true });
+      component["delayedAskForBiometric"] = jest.fn();
+      await component.ngOnInit();
+
+      expect(component["delayedAskForBiometric"]).toHaveBeenCalledTimes(1);
+      expect(component["delayedAskForBiometric"]).toHaveBeenCalledWith(500);
+    });
+
+    it("should call messagingService.send", async () => {
+      await component.ngOnInit();
+      expect(messagingServiceMock.send).toHaveBeenCalledWith("getWindowIsFocused");
+    });
+
+    describe("broadcasterService.subscribe", () => {
+      it('should call onWindowHidden() when "broadcasterService.subscribe" is called with "windowHidden"', async () => {
+        component["onWindowHidden"] = jest.fn();
+        await component.ngOnInit();
+        broadcasterServiceMock.subscribe.mock.calls[0][1]({ command: "windowHidden" });
+        expect(component["onWindowHidden"]).toHaveBeenCalledTimes(1);
+      });
+
+      it('should call focusInput() when "broadcasterService.subscribe" is called with "windowIsFocused" is true and deferFocus is false', async () => {
+        component["focusInput"] = jest.fn();
+        component["deferFocus"] = null;
+        await component.ngOnInit();
+        broadcasterServiceMock.subscribe.mock.calls[0][1]({
+          command: "windowIsFocused",
+          windowIsFocused: true,
+        } as any);
+        expect(component["deferFocus"]).toBe(false);
+        expect(component["focusInput"]).toHaveBeenCalledTimes(1);
+      });
+
+      it('should not call focusInput() when "broadcasterService.subscribe" is called with "windowIsFocused" is true and deferFocus is true', async () => {
+        component["focusInput"] = jest.fn();
+        component["deferFocus"] = null;
+        await component.ngOnInit();
+        broadcasterServiceMock.subscribe.mock.calls[0][1]({
+          command: "windowIsFocused",
+          windowIsFocused: false,
+        } as any);
+        expect(component["deferFocus"]).toBe(true);
+        expect(component["focusInput"]).toHaveBeenCalledTimes(0);
+      });
+
+      it('should call focusInput() when "broadcasterService.subscribe" is called with "windowIsFocused" is true and deferFocus is true', async () => {
+        component["focusInput"] = jest.fn();
+        component["deferFocus"] = true;
+        await component.ngOnInit();
+        broadcasterServiceMock.subscribe.mock.calls[0][1]({
+          command: "windowIsFocused",
+          windowIsFocused: true,
+        } as any);
+        expect(component["deferFocus"]).toBe(false);
+        expect(component["focusInput"]).toHaveBeenCalledTimes(1);
+      });
+
+      it('should not call focusInput() when "broadcasterService.subscribe" is called with "windowIsFocused" is false and deferFocus is true', async () => {
+        component["focusInput"] = jest.fn();
+        component["deferFocus"] = true;
+        await component.ngOnInit();
+        broadcasterServiceMock.subscribe.mock.calls[0][1]({
+          command: "windowIsFocused",
+          windowIsFocused: false,
+        } as any);
+        expect(component["deferFocus"]).toBe(true);
+        expect(component["focusInput"]).toHaveBeenCalledTimes(0);
+      });
+    });
+  });
+
+  describe("ngOnDestroy", () => {
+    it("should call super.ngOnDestroy()", () => {
+      const superNgOnDestroySpy = jest.spyOn(BaseLockComponent.prototype, "ngOnDestroy");
+      component.ngOnDestroy();
+      expect(superNgOnDestroySpy).toHaveBeenCalledTimes(1);
+    });
+
+    it("should call broadcasterService.unsubscribe()", () => {
+      component.ngOnDestroy();
+      expect(broadcasterServiceMock.unsubscribe).toHaveBeenCalledTimes(1);
+    });
+  });
+
+  describe("focusInput", () => {
+    it('should call "focus" on #pin input if pinEnabled is true', () => {
+      component["pinEnabled"] = true;
+      global.document.getElementById = jest.fn().mockReturnValue({ focus: jest.fn() });
+      component["focusInput"]();
+      expect(global.document.getElementById).toHaveBeenCalledWith("pin");
+    });
+
+    it('should call "focus" on #masterPassword input if pinEnabled is false', () => {
+      component["pinEnabled"] = false;
+      global.document.getElementById = jest.fn().mockReturnValue({ focus: jest.fn() });
+      component["focusInput"]();
+      expect(global.document.getElementById).toHaveBeenCalledWith("masterPassword");
+    });
+  });
+
+  describe("delayedAskForBiometric", () => {
+    beforeEach(() => {
+      component["supportsBiometric"] = true;
+      component["autoPromptBiometric"] = true;
+    });
+
+    it('should wait for "delay" milliseconds', fakeAsync(async () => {
+      const delaySpy = jest.spyOn(global, "setTimeout");
+      component["delayedAskForBiometric"](5000);
+
+      tick(4000);
+      component["biometricAsked"] = false;
+
+      tick(1000);
+      component["biometricAsked"] = true;
+
+      expect(delaySpy).toHaveBeenCalledWith(expect.any(Function), 5000);
+    }));
+
+    it('should return; if "params" is defined and "params.promptBiometric" is false', fakeAsync(async () => {
+      component["delayedAskForBiometric"](5000, { promptBiometric: false });
+      tick(5000);
+      expect(component["biometricAsked"]).toBe(false);
+    }));
+
+    it('should not return; if "params" is defined and "params.promptBiometric" is true', fakeAsync(async () => {
+      component["delayedAskForBiometric"](5000, { promptBiometric: true });
+      tick(5000);
+      expect(component["biometricAsked"]).toBe(true);
+    }));
+
+    it('should not return; if "params" is undefined', fakeAsync(async () => {
+      component["delayedAskForBiometric"](5000);
+      tick(5000);
+      expect(component["biometricAsked"]).toBe(true);
+    }));
+
+    it('should return; if "supportsBiometric" is false', fakeAsync(async () => {
+      component["supportsBiometric"] = false;
+      component["delayedAskForBiometric"](5000);
+      tick(5000);
+      expect(component["biometricAsked"]).toBe(false);
+    }));
+
+    it('should return; if "autoPromptBiometric" is false', fakeAsync(async () => {
+      component["autoPromptBiometric"] = false;
+      component["delayedAskForBiometric"](5000);
+      tick(5000);
+      expect(component["biometricAsked"]).toBe(false);
+    }));
+
+    it("should call unlockBiometric() if biometricAsked is false and window is visible", fakeAsync(async () => {
+      isWindowVisibleMock.mockResolvedValue(true);
+      component["unlockBiometric"] = jest.fn();
+      component["biometricAsked"] = false;
+      component["delayedAskForBiometric"](5000);
+      tick(5000);
+
+      expect(component["unlockBiometric"]).toHaveBeenCalledTimes(1);
+    }));
+
+    it("should not call unlockBiometric() if biometricAsked is false and window is not visible", fakeAsync(async () => {
+      isWindowVisibleMock.mockResolvedValue(false);
+      component["unlockBiometric"] = jest.fn();
+      component["biometricAsked"] = false;
+      component["delayedAskForBiometric"](5000);
+      tick(5000);
+
+      expect(component["unlockBiometric"]).toHaveBeenCalledTimes(0);
+    }));
+
+    it("should not call unlockBiometric() if biometricAsked is true", fakeAsync(async () => {
+      isWindowVisibleMock.mockResolvedValue(true);
+      component["unlockBiometric"] = jest.fn();
+      component["biometricAsked"] = true;
+
+      component["delayedAskForBiometric"](5000);
+      tick(5000);
+
+      expect(component["unlockBiometric"]).toHaveBeenCalledTimes(0);
+    }));
+  });
+
+  describe("canUseBiometric", () => {
+    it("should call getUserId() on stateService", async () => {
+      stateServiceMock.getUserId.mockResolvedValue("userId");
+      await component["canUseBiometric"]();
+
+      expect(ipc.platform.biometric.enabled).toHaveBeenCalledWith("userId");
+    });
+  });
+
+  it('onWindowHidden() should set "showPassword" to false', () => {
+    component["showPassword"] = true;
+    component["onWindowHidden"]();
+    expect(component["showPassword"]).toBe(false);
+  });
+});
diff --git a/apps/desktop/src/auth/lock.component.ts b/apps/desktop/src/auth/lock.component.ts
index 91a60557fb9..3f62df7dd1c 100644
--- a/apps/desktop/src/auth/lock.component.ts
+++ b/apps/desktop/src/auth/lock.component.ts
@@ -1,5 +1,6 @@
 import { Component, NgZone } from "@angular/core";
 import { ActivatedRoute, Router } from "@angular/router";
+import { switchMap } from "rxjs";
 
 import { LockComponent as BaseLockComponent } from "@bitwarden/angular/auth/components/lock.component";
 import { ApiService } from "@bitwarden/common/abstractions/api.service";
@@ -31,6 +32,8 @@ const BroadcasterSubscriptionId = "LockComponent";
 export class LockComponent extends BaseLockComponent {
   private deferFocus: boolean = null;
   protected biometricReady = false;
+  private biometricAsked = false;
+  private autoPromptBiometric = false;
 
   constructor(
     router: Router,
@@ -78,23 +81,14 @@ export class LockComponent extends BaseLockComponent {
 
   async ngOnInit() {
     await super.ngOnInit();
-    const autoPromptBiometric = !(await this.stateService.getDisableAutoBiometricsPrompt());
+    this.autoPromptBiometric = !(await this.stateService.getDisableAutoBiometricsPrompt());
     this.biometricReady = await this.canUseBiometric();
 
     await this.displayBiometricUpdateWarning();
 
-    // eslint-disable-next-line rxjs-angular/prefer-takeuntil
-    this.route.queryParams.subscribe((params) => {
-      setTimeout(async () => {
-        if (!params.promptBiometric || !this.supportsBiometric || !autoPromptBiometric) {
-          return;
-        }
+    this.delayedAskForBiometric(500);
+    this.route.queryParams.pipe(switchMap((params) => this.delayedAskForBiometric(500, params)));
 
-        if (await ipc.platform.isWindowVisible()) {
-          this.unlockBiometric();
-        }
-      }, 1000);
-    });
     this.broadcasterService.subscribe(BroadcasterSubscriptionId, async (message: any) => {
       this.ngZone.run(() => {
         switch (message.command) {
@@ -128,6 +122,23 @@ export class LockComponent extends BaseLockComponent {
     this.showPassword = false;
   }
 
+  private async delayedAskForBiometric(delay: number, params?: any) {
+    await new Promise((resolve) => setTimeout(resolve, delay));
+
+    if (params && !params.promptBiometric) {
+      return;
+    }
+
+    if (!this.supportsBiometric || !this.autoPromptBiometric || this.biometricAsked) {
+      return;
+    }
+
+    this.biometricAsked = true;
+    if (await ipc.platform.isWindowVisible()) {
+      this.unlockBiometric();
+    }
+  }
+
   private async canUseBiometric() {
     const userId = await this.stateService.getUserId();
     return await ipc.platform.biometric.enabled(userId);
diff --git a/apps/web/src/app/auth/core/services/webauthn-login/request/enable-credential-encryption.request.ts b/apps/web/src/app/auth/core/services/webauthn-login/request/enable-credential-encryption.request.ts
new file mode 100644
index 00000000000..6dc08728ad1
--- /dev/null
+++ b/apps/web/src/app/auth/core/services/webauthn-login/request/enable-credential-encryption.request.ts
@@ -0,0 +1,25 @@
+import { WebAuthnLoginAssertionResponseRequest } from "@bitwarden/common/auth/services/webauthn-login/request/webauthn-login-assertion-response.request";
+
+/**
+ * Request sent to the server to save a newly created prf key set for a credential.
+ */
+export class EnableCredentialEncryptionRequest {
+  /**
+   * The response received from the authenticator.
+   */
+  deviceResponse: WebAuthnLoginAssertionResponseRequest;
+
+  /**
+   * An encrypted token containing information the server needs to verify the credential.
+   */
+  token: string;
+
+  /** Used for vault encryption. See {@link RotateableKeySet.encryptedUserKey } */
+  encryptedUserKey?: string;
+
+  /** Used for vault encryption. See {@link RotateableKeySet.encryptedPublicKey } */
+  encryptedPublicKey?: string;
+
+  /** Used for vault encryption. See {@link RotateableKeySet.encryptedPrivateKey } */
+  encryptedPrivateKey?: string;
+}
diff --git a/apps/web/src/app/auth/core/services/webauthn-login/request/webauthn-login-attestation-response.request.ts b/apps/web/src/app/auth/core/services/webauthn-login/request/webauthn-login-attestation-response.request.ts
index 249b2ebffa9..ef3d657f2f9 100644
--- a/apps/web/src/app/auth/core/services/webauthn-login/request/webauthn-login-attestation-response.request.ts
+++ b/apps/web/src/app/auth/core/services/webauthn-login/request/webauthn-login-attestation-response.request.ts
@@ -3,7 +3,7 @@ import { Utils } from "@bitwarden/common/platform/misc/utils";
 import { WebauthnLoginAuthenticatorResponseRequest } from "./webauthn-login-authenticator-response.request";
 
 /**
- * The response received from an authentiator after a successful attestation.
+ * The response received from an authenticator after a successful attestation.
  * This request is used to save newly created webauthn login credentials to the server.
  */
 export class WebauthnLoginAttestationResponseRequest extends WebauthnLoginAuthenticatorResponseRequest {
diff --git a/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin-api.service.ts b/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin-api.service.ts
index 8b99396b0fb..efa32d0c6fe 100644
--- a/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin-api.service.ts
+++ b/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin-api.service.ts
@@ -2,8 +2,10 @@ import { Injectable } from "@angular/core";
 
 import { ApiService } from "@bitwarden/common/abstractions/api.service";
 import { SecretVerificationRequest } from "@bitwarden/common/auth/models/request/secret-verification.request";
+import { CredentialAssertionOptionsResponse } from "@bitwarden/common/auth/services/webauthn-login/response/credential-assertion-options.response";
 import { ListResponse } from "@bitwarden/common/models/response/list.response";
 
+import { EnableCredentialEncryptionRequest } from "./request/enable-credential-encryption.request";
 import { SaveCredentialRequest } from "./request/save-credential.request";
 import { WebauthnLoginCredentialCreateOptionsResponse } from "./response/webauthn-login-credential-create-options.response";
 import { WebauthnLoginCredentialResponse } from "./response/webauthn-login-credential.response";
@@ -15,10 +17,29 @@ export class WebAuthnLoginAdminApiService {
   async getCredentialCreateOptions(
     request: SecretVerificationRequest,
   ): Promise<WebauthnLoginCredentialCreateOptionsResponse> {
-    const response = await this.apiService.send("POST", "/webauthn/options", request, true, true);
+    const response = await this.apiService.send(
+      "POST",
+      "/webauthn/attestation-options",
+      request,
+      true,
+      true,
+    );
     return new WebauthnLoginCredentialCreateOptionsResponse(response);
   }
 
+  async getCredentialAssertionOptions(
+    request: SecretVerificationRequest,
+  ): Promise<CredentialAssertionOptionsResponse> {
+    const response = await this.apiService.send(
+      "POST",
+      "/webauthn/assertion-options",
+      request,
+      true,
+      true,
+    );
+    return new CredentialAssertionOptionsResponse(response);
+  }
+
   async saveCredential(request: SaveCredentialRequest): Promise<boolean> {
     await this.apiService.send("POST", "/webauthn", request, true, true);
     return true;
@@ -31,4 +52,8 @@ export class WebAuthnLoginAdminApiService {
   async deleteCredential(credentialId: string, request: SecretVerificationRequest): Promise<void> {
     await this.apiService.send("POST", `/webauthn/${credentialId}/delete`, request, true, true);
   }
+
+  async updateCredential(request: EnableCredentialEncryptionRequest): Promise<void> {
+    await this.apiService.send("PUT", `/webauthn`, request, true, true);
+  }
 }
diff --git a/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.spec.ts b/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.spec.ts
index 49c1f89052b..bc92114e878 100644
--- a/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.spec.ts
+++ b/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.spec.ts
@@ -1,12 +1,21 @@
+import { randomBytes } from "crypto";
+
 import { mock, MockProxy } from "jest-mock-extended";
 
+import { RotateableKeySet } from "@bitwarden/auth";
 import { UserVerificationService } from "@bitwarden/common/auth/abstractions/user-verification/user-verification.service.abstraction";
 import { WebAuthnLoginPrfCryptoServiceAbstraction } from "@bitwarden/common/auth/abstractions/webauthn/webauthn-login-prf-crypto.service.abstraction";
+import { WebAuthnLoginCredentialAssertionView } from "@bitwarden/common/auth/models/view/webauthn-login/webauthn-login-credential-assertion.view";
+import { WebAuthnLoginAssertionResponseRequest } from "@bitwarden/common/auth/services/webauthn-login/request/webauthn-login-assertion-response.request";
+import { Utils } from "@bitwarden/common/platform/misc/utils";
+import { EncString } from "@bitwarden/common/platform/models/domain/enc-string";
+import { PrfKey } from "@bitwarden/common/platform/models/domain/symmetric-crypto-key";
 
 import { CredentialCreateOptionsView } from "../../views/credential-create-options.view";
 import { PendingWebauthnLoginCredentialView } from "../../views/pending-webauthn-login-credential.view";
 import { RotateableKeySetService } from "../rotateable-key-set.service";
 
+import { EnableCredentialEncryptionRequest } from "./request/enable-credential-encryption.request";
 import { WebAuthnLoginAdminApiService } from "./webauthn-login-admin-api.service";
 import { WebauthnLoginAdminService } from "./webauthn-login-admin.service";
 
@@ -18,10 +27,13 @@ describe("WebauthnAdminService", () => {
   let credentials: MockProxy<CredentialsContainer>;
   let service!: WebauthnLoginAdminService;
 
+  let originalAuthenticatorAssertionResponse!: AuthenticatorAssertionResponse | any;
+
   beforeAll(() => {
     // Polyfill missing class
     window.PublicKeyCredential = class {} as any;
     window.AuthenticatorAttestationResponse = class {} as any;
+    window.AuthenticatorAssertionResponse = class {} as any;
     apiService = mock<WebAuthnLoginAdminApiService>();
     userVerificationService = mock<UserVerificationService>();
     rotateableKeySetService = mock<RotateableKeySetService>();
@@ -34,6 +46,20 @@ describe("WebauthnAdminService", () => {
       webAuthnLoginPrfCryptoService,
       credentials,
     );
+
+    // Save original global class
+    originalAuthenticatorAssertionResponse = global.AuthenticatorAssertionResponse;
+    // Mock the global AuthenticatorAssertionResponse class b/c the class is only available in secure contexts
+    global.AuthenticatorAssertionResponse = MockAuthenticatorAssertionResponse;
+  });
+
+  beforeEach(() => {
+    jest.clearAllMocks();
+  });
+
+  afterAll(() => {
+    // Restore global after all tests are done
+    global.AuthenticatorAssertionResponse = originalAuthenticatorAssertionResponse;
   });
 
   describe("createCredential", () => {
@@ -70,6 +96,94 @@ describe("WebauthnAdminService", () => {
       expect(result.supportsPrf).toBe(true);
     });
   });
+
+  describe("enableCredentialEncryption", () => {
+    it("should call the necessary methods to update the credential", async () => {
+      // Arrange
+      const response = new MockPublicKeyCredential();
+      const prfKeySet = new RotateableKeySet<PrfKey>(
+        new EncString("test_encryptedUserKey"),
+        new EncString("test_encryptedPublicKey"),
+        new EncString("test_encryptedPrivateKey"),
+      );
+
+      const assertionOptions: WebAuthnLoginCredentialAssertionView =
+        new WebAuthnLoginCredentialAssertionView(
+          "enable_credential_encryption_test_token",
+          new WebAuthnLoginAssertionResponseRequest(response),
+          {} as PrfKey,
+        );
+
+      const request = new EnableCredentialEncryptionRequest();
+      request.token = assertionOptions.token;
+      request.deviceResponse = assertionOptions.deviceResponse;
+      request.encryptedUserKey = prfKeySet.encryptedUserKey.encryptedString;
+      request.encryptedPublicKey = prfKeySet.encryptedPublicKey.encryptedString;
+      request.encryptedPrivateKey = prfKeySet.encryptedPrivateKey.encryptedString;
+
+      // Mock the necessary methods and services
+      const createKeySetMock = jest
+        .spyOn(rotateableKeySetService, "createKeySet")
+        .mockResolvedValue(prfKeySet);
+      const updateCredentialMock = jest.spyOn(apiService, "updateCredential").mockResolvedValue();
+
+      // Act
+      await service.enableCredentialEncryption(assertionOptions);
+
+      // Assert
+      expect(createKeySetMock).toHaveBeenCalledWith(assertionOptions.prfKey);
+      expect(updateCredentialMock).toHaveBeenCalledWith(request);
+    });
+
+    it("should throw error when PRF Key is undefined", async () => {
+      // Arrange
+      const response = new MockPublicKeyCredential();
+
+      const assertionOptions: WebAuthnLoginCredentialAssertionView =
+        new WebAuthnLoginCredentialAssertionView(
+          "enable_credential_encryption_test_token",
+          new WebAuthnLoginAssertionResponseRequest(response),
+          undefined,
+        );
+
+      // Mock the necessary methods and services
+      const createKeySetMock = jest
+        .spyOn(rotateableKeySetService, "createKeySet")
+        .mockResolvedValue(null);
+      const updateCredentialMock = jest.spyOn(apiService, "updateCredential").mockResolvedValue();
+
+      // Act
+      try {
+        await service.enableCredentialEncryption(assertionOptions);
+      } catch (error) {
+        // Assert
+        expect(error).toEqual(new Error("invalid credential"));
+        expect(createKeySetMock).not.toHaveBeenCalled();
+        expect(updateCredentialMock).not.toHaveBeenCalled();
+      }
+    });
+
+    it("should throw error when WehAuthnLoginCredentialAssertionView is undefined", async () => {
+      // Arrange
+      const assertionOptions: WebAuthnLoginCredentialAssertionView = undefined;
+
+      // Mock the necessary methods and services
+      const createKeySetMock = jest
+        .spyOn(rotateableKeySetService, "createKeySet")
+        .mockResolvedValue(null);
+      const updateCredentialMock = jest.spyOn(apiService, "updateCredential").mockResolvedValue();
+
+      // Act
+      try {
+        await service.enableCredentialEncryption(assertionOptions);
+      } catch (error) {
+        // Assert
+        expect(error).toEqual(new Error("invalid credential"));
+        expect(createKeySetMock).not.toHaveBeenCalled();
+        expect(updateCredentialMock).not.toHaveBeenCalled();
+      }
+    });
+  });
 });
 
 function createCredentialCreateOptions(): CredentialCreateOptionsView {
@@ -115,3 +229,58 @@ function createDeviceResponse({ prf = false }: { prf?: boolean } = {}): PublicKe
 
   return credential;
 }
+
+/**
+ * Mocks for the PublicKeyCredential and AuthenticatorAssertionResponse classes copied from webauthn-login.service.spec.ts
+ */
+
+// AuthenticatorAssertionResponse && PublicKeyCredential are only available in secure contexts
+// so we need to mock them and assign them to the global object to make them available
+// for the tests
+class MockAuthenticatorAssertionResponse implements AuthenticatorAssertionResponse {
+  clientDataJSON: ArrayBuffer = randomBytes(32).buffer;
+  authenticatorData: ArrayBuffer = randomBytes(196).buffer;
+  signature: ArrayBuffer = randomBytes(72).buffer;
+  userHandle: ArrayBuffer = randomBytes(16).buffer;
+
+  clientDataJSONB64Str = Utils.fromBufferToUrlB64(this.clientDataJSON);
+  authenticatorDataB64Str = Utils.fromBufferToUrlB64(this.authenticatorData);
+  signatureB64Str = Utils.fromBufferToUrlB64(this.signature);
+  userHandleB64Str = Utils.fromBufferToUrlB64(this.userHandle);
+}
+
+class MockPublicKeyCredential implements PublicKeyCredential {
+  authenticatorAttachment = "cross-platform";
+  id = "mockCredentialId";
+  type = "public-key";
+  rawId: ArrayBuffer = randomBytes(32).buffer;
+  rawIdB64Str = Utils.fromBufferToUrlB64(this.rawId);
+
+  response: MockAuthenticatorAssertionResponse = new MockAuthenticatorAssertionResponse();
+
+  // Use random 64 character hex string (32 bytes - matters for symmetric key creation)
+  // to represent the prf key binary data and convert to ArrayBuffer
+  // Creating the array buffer from a known hex value allows us to
+  // assert on the value in tests
+  private prfKeyArrayBuffer: ArrayBuffer = Utils.hexStringToArrayBuffer(
+    "1234567890abcdef1234567890abcdef1234567890abcdef1234567890abcdef",
+  );
+
+  getClientExtensionResults(): any {
+    return {
+      prf: {
+        results: {
+          first: this.prfKeyArrayBuffer,
+        },
+      },
+    };
+  }
+
+  static isConditionalMediationAvailable(): Promise<boolean> {
+    return Promise.resolve(false);
+  }
+
+  static isUserVerifyingPlatformAuthenticatorAvailable(): Promise<boolean> {
+    return Promise.resolve(false);
+  }
+}
diff --git a/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.ts b/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.ts
index 1fee82c74be..a59b2395e11 100644
--- a/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.ts
+++ b/apps/web/src/app/auth/core/services/webauthn-login/webauthn-login-admin.service.ts
@@ -4,6 +4,8 @@ import { BehaviorSubject, filter, from, map, Observable, shareReplay, switchMap,
 import { PrfKeySet } from "@bitwarden/auth";
 import { UserVerificationService } from "@bitwarden/common/auth/abstractions/user-verification/user-verification.service.abstraction";
 import { WebAuthnLoginPrfCryptoServiceAbstraction } from "@bitwarden/common/auth/abstractions/webauthn/webauthn-login-prf-crypto.service.abstraction";
+import { WebAuthnLoginCredentialAssertionOptionsView } from "@bitwarden/common/auth/models/view/webauthn-login/webauthn-login-credential-assertion-options.view";
+import { WebAuthnLoginCredentialAssertionView } from "@bitwarden/common/auth/models/view/webauthn-login/webauthn-login-credential-assertion.view";
 import { Verification } from "@bitwarden/common/auth/types/verification";
 import { LogService } from "@bitwarden/common/platform/abstractions/log.service";
 
@@ -12,6 +14,7 @@ import { PendingWebauthnLoginCredentialView } from "../../views/pending-webauthn
 import { WebauthnLoginCredentialView } from "../../views/webauthn-login-credential.view";
 import { RotateableKeySetService } from "../rotateable-key-set.service";
 
+import { EnableCredentialEncryptionRequest } from "./request/enable-credential-encryption.request";
 import { SaveCredentialRequest } from "./request/save-credential.request";
 import { WebauthnLoginAttestationResponseRequest } from "./request/webauthn-login-attestation-response.request";
 import { WebAuthnLoginAdminApiService } from "./webauthn-login-admin-api.service";
@@ -52,14 +55,31 @@ export class WebauthnLoginAdminService {
   }
 
   /**
-   * Get the credential attestation options needed for initiating the WebAuthnLogin credentail creation process.
+   * Get the credential assertion options needed for initiating the WebAuthnLogin credential update process.
+   * The options contains assertion options and other data for the authenticator.
+   * This method requires user verification.
+   *
+   * @param verification User verification data to be used for the request.
+   * @returns The credential assertion options and a token to be used for the credential update request.
+   */
+  async getCredentialAssertOptions(
+    verification: Verification,
+  ): Promise<WebAuthnLoginCredentialAssertionOptionsView> {
+    const request = await this.userVerificationService.buildRequest(verification);
+    const response = await this.apiService.getCredentialAssertionOptions(request);
+    return new WebAuthnLoginCredentialAssertionOptionsView(response.options, response.token);
+  }
+
+  /**
+   * Get the credential attestation options needed for initiating the WebAuthnLogin credential creation process.
    * The options contains a challenge and other data for the authenticator.
    * This method requires user verification.
    *
    * @param verification User verification data to be used for the request.
    * @returns The credential attestation options and a token to be used for the credential creation request.
    */
-  async getCredentialCreateOptions(
+
+  async getCredentialAttestationOptions(
     verification: Verification,
   ): Promise<CredentialCreateOptionsView> {
     const request = await this.userVerificationService.buildRequest(verification);
@@ -169,6 +189,36 @@ export class WebauthnLoginAdminService {
     this.refresh();
   }
 
+  /**
+   * Enable encryption for a credential that has already been saved to the server.
+   * This will update the KeySet associated with the credential in the database.
+   * We short circuit the process here incase the WebAuthnLoginCredential doesn't support PRF or
+   * if there was a problem with the Credential Assertion.
+   *
+   * @param assertionOptions Options received from the server using `getCredentialAssertOptions`.
+   * @returns void
+   */
+  async enableCredentialEncryption(
+    assertionOptions: WebAuthnLoginCredentialAssertionView,
+  ): Promise<void> {
+    if (assertionOptions === undefined || assertionOptions?.prfKey === undefined) {
+      throw new Error("invalid credential");
+    }
+
+    const prfKeySet: PrfKeySet = await this.rotateableKeySetService.createKeySet(
+      assertionOptions.prfKey,
+    );
+
+    const request = new EnableCredentialEncryptionRequest();
+    request.token = assertionOptions.token;
+    request.deviceResponse = assertionOptions.deviceResponse;
+    request.encryptedUserKey = prfKeySet.encryptedUserKey.encryptedString;
+    request.encryptedPublicKey = prfKeySet.encryptedPublicKey.encryptedString;
+    request.encryptedPrivateKey = prfKeySet.encryptedPrivateKey.encryptedString;
+    await this.apiService.updateCredential(request);
+    this.refresh();
+  }
+
   /**
    * List of webauthn credentials saved on the server.
    *
diff --git a/apps/web/src/app/auth/settings/webauthn-login-settings/create-credential-dialog/create-credential-dialog.component.ts b/apps/web/src/app/auth/settings/webauthn-login-settings/create-credential-dialog/create-credential-dialog.component.ts
index fcb0e995f4a..4c5198ea132 100644
--- a/apps/web/src/app/auth/settings/webauthn-login-settings/create-credential-dialog/create-credential-dialog.component.ts
+++ b/apps/web/src/app/auth/settings/webauthn-login-settings/create-credential-dialog/create-credential-dialog.component.ts
@@ -94,7 +94,7 @@ export class CreateCredentialDialogComponent implements OnInit {
     }
 
     try {
-      this.credentialOptions = await this.webauthnService.getCredentialCreateOptions(
+      this.credentialOptions = await this.webauthnService.getCredentialAttestationOptions(
         this.formGroup.value.userVerification.secret,
       );
     } catch (error) {
diff --git a/apps/web/src/app/auth/settings/webauthn-login-settings/enable-encryption-dialog/enable-encryption-dialog.component.html b/apps/web/src/app/auth/settings/webauthn-login-settings/enable-encryption-dialog/enable-encryption-dialog.component.html
new file mode 100644
index 00000000000..3fe6f43a052
--- /dev/null
+++ b/apps/web/src/app/auth/settings/webauthn-login-settings/enable-encryption-dialog/enable-encryption-dialog.component.html
@@ -0,0 +1,34 @@
+<form [formGroup]="formGroup" [bitSubmit]="submit">
+  <bit-dialog dialogSize="large" [loading]="loading$ | async">
+    <span bitDialogTitle
+      >{{ "enablePasskeyEncryption" | i18n }}
+      <span *ngIf="credential" class="tw-text-sm tw-normal-case tw-text-muted">{{
+        credential.name
+      }}</span>
+    </span>
+    <ng-container bitDialogContent>
+      <ng-container *ngIf="!credential">
+        <i class="bwi bwi-spinner bwi-spin tw-ml-1" aria-hidden="true"></i>
+      </ng-container>
+
+      <ng-container *ngIf="credential">
+        <p bitTypography="body1">{{ "useForVaultEncryptionInfo" | i18n }}</p>
+
+        <ng-container formGroupName="userVerification">
+          <app-user-verification
+            formControlName="secret"
+            [(invalidSecret)]="invalidSecret"
+          ></app-user-verification>
+        </ng-container>
+      </ng-container>
+    </ng-container>
+    <ng-container bitDialogFooter>
+      <button type="submit" bitButton bitFormButton buttonType="primary">
+        {{ "submit" | i18n }}
+      </button>
+      <button type="button" bitButton bitFormButton buttonType="secondary" bitDialogClose>
+        {{ "cancel" | i18n }}
+      </button>
+    </ng-container>
+  </bit-dialog>
+</form>
diff --git a/apps/web/src/app/auth/settings/webauthn-login-settings/enable-encryption-dialog/enable-encryption-dialog.component.ts b/apps/web/src/app/auth/settings/webauthn-login-settings/enable-encryption-dialog/enable-encryption-dialog.component.ts
new file mode 100644
index 00000000000..741b71abcf2
--- /dev/null
+++ b/apps/web/src/app/auth/settings/webauthn-login-settings/enable-encryption-dialog/enable-encryption-dialog.component.ts
@@ -0,0 +1,91 @@
+import { DIALOG_DATA, DialogConfig, DialogRef } from "@angular/cdk/dialog";
+import { Component, Inject, OnDestroy, OnInit } from "@angular/core";
+import { FormBuilder, Validators } from "@angular/forms";
+import { Subject } from "rxjs";
+import { takeUntil } from "rxjs/operators";
+
+import { WebAuthnLoginServiceAbstraction } from "@bitwarden/common/auth/abstractions/webauthn/webauthn-login.service.abstraction";
+import { WebAuthnLoginCredentialAssertionOptionsView } from "@bitwarden/common/auth/models/view/webauthn-login/webauthn-login-credential-assertion-options.view";
+import { Verification } from "@bitwarden/common/auth/types/verification";
+import { ErrorResponse } from "@bitwarden/common/models/response/error.response";
+import { DialogService } from "@bitwarden/components/src/dialog/dialog.service";
+
+import { WebauthnLoginAdminService } from "../../../core/services/webauthn-login/webauthn-login-admin.service";
+import { WebauthnLoginCredentialView } from "../../../core/views/webauthn-login-credential.view";
+
+export interface EnableEncryptionDialogParams {
+  credentialId: string;
+}
+
+@Component({
+  templateUrl: "enable-encryption-dialog.component.html",
+})
+export class EnableEncryptionDialogComponent implements OnInit, OnDestroy {
+  private destroy$ = new Subject<void>();
+
+  protected invalidSecret = false;
+  protected formGroup = this.formBuilder.group({
+    userVerification: this.formBuilder.group({
+      secret: [null as Verification | null, Validators.required],
+    }),
+  });
+
+  protected credential?: WebauthnLoginCredentialView;
+  protected credentialOptions?: WebAuthnLoginCredentialAssertionOptionsView;
+  protected loading$ = this.webauthnService.loading$;
+
+  constructor(
+    @Inject(DIALOG_DATA) private params: EnableEncryptionDialogParams,
+    private formBuilder: FormBuilder,
+    private dialogRef: DialogRef,
+    private webauthnService: WebauthnLoginAdminService,
+    private webauthnLoginService: WebAuthnLoginServiceAbstraction,
+  ) {}
+
+  ngOnInit(): void {
+    this.webauthnService
+      .getCredential$(this.params.credentialId)
+      .pipe(takeUntil(this.destroy$))
+      .subscribe((credential: any) => (this.credential = credential));
+  }
+
+  submit = async () => {
+    if (this.credential === undefined) {
+      return;
+    }
+
+    this.dialogRef.disableClose = true;
+    try {
+      this.credentialOptions = await this.webauthnService.getCredentialAssertOptions(
+        this.formGroup.value.userVerification.secret,
+      );
+      await this.webauthnService.enableCredentialEncryption(
+        await this.webauthnLoginService.assertCredential(this.credentialOptions),
+      );
+    } catch (error) {
+      if (error instanceof ErrorResponse && error.statusCode === 400) {
+        this.invalidSecret = true;
+      }
+      throw error;
+    }
+
+    this.dialogRef.close();
+  };
+
+  ngOnDestroy(): void {
+    this.destroy$.next();
+    this.destroy$.complete();
+  }
+}
+
+/**
+ * Strongly typed helper to open a EnableEncryptionDialogComponent
+ * @param dialogService Instance of the dialog service that will be used to open the dialog
+ * @param config Configuration for the dialog
+ */
+export const openEnableCredentialDialogComponent = (
+  dialogService: DialogService,
+  config: DialogConfig<EnableEncryptionDialogParams>,
+) => {
+  return dialogService.open<unknown>(EnableEncryptionDialogComponent, config);
+};
diff --git a/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.html b/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.html
index dc55be99f1b..968b8565a6f 100644
--- a/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.html
+++ b/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.html
@@ -39,8 +39,16 @@
         <span bitTypography="body1" class="tw-text-muted">{{ "usedForEncryption" | i18n }}</span>
       </ng-container>
       <ng-container *ngIf="credential.prfStatus === WebauthnLoginCredentialPrfStatus.Supported">
-        <i class="bwi bwi-lock-encrypted"></i>
-        <span bitTypography="body1" class="tw-text-muted">{{ "encryptionNotEnabled" | i18n }}</span>
+        <button
+          type="button"
+          bitLink
+          [disabled]="loading"
+          [attr.aria-label]="('enablePasskeyEncryption' | i18n) + ' ' + credential.name"
+          (click)="enableEncryption(credential.id)"
+        >
+          <i class="bwi bwi-lock-encrypted"></i>
+          {{ "enablePasskeyEncryption" | i18n }}
+        </button>
       </ng-container>
       <span
         *ngIf="credential.prfStatus === WebauthnLoginCredentialPrfStatus.Unsupported"
diff --git a/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.ts b/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.ts
index 140f1530483..db7d8f81d1a 100644
--- a/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.ts
+++ b/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.component.ts
@@ -11,6 +11,7 @@ import { WebauthnLoginCredentialView } from "../../core/views/webauthn-login-cre
 
 import { openCreateCredentialDialog } from "./create-credential-dialog/create-credential-dialog.component";
 import { openDeleteCredentialDialogComponent } from "./delete-credential-dialog/delete-credential-dialog.component";
+import { openEnableCredentialDialogComponent } from "./enable-encryption-dialog/enable-encryption-dialog.component";
 
 @Component({
   selector: "app-webauthn-login-settings",
@@ -83,4 +84,8 @@ export class WebauthnLoginSettingsComponent implements OnInit, OnDestroy {
   protected deleteCredential(credentialId: string) {
     openDeleteCredentialDialogComponent(this.dialogService, { data: { credentialId } });
   }
+
+  protected enableEncryption(credentialId: string) {
+    openEnableCredentialDialogComponent(this.dialogService, { data: { credentialId } });
+  }
 }
diff --git a/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.module.ts b/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.module.ts
index 191f8d354b6..75433eea7fb 100644
--- a/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.module.ts
+++ b/apps/web/src/app/auth/settings/webauthn-login-settings/webauthn-login-settings.module.ts
@@ -8,6 +8,7 @@ import { UserVerificationModule } from "../../shared/components/user-verificatio
 
 import { CreateCredentialDialogComponent } from "./create-credential-dialog/create-credential-dialog.component";
 import { DeleteCredentialDialogComponent } from "./delete-credential-dialog/delete-credential-dialog.component";
+import { EnableEncryptionDialogComponent } from "./enable-encryption-dialog/enable-encryption-dialog.component";
 import { WebauthnLoginSettingsComponent } from "./webauthn-login-settings.component";
 
 @NgModule({
@@ -16,6 +17,7 @@ import { WebauthnLoginSettingsComponent } from "./webauthn-login-settings.compon
     WebauthnLoginSettingsComponent,
     CreateCredentialDialogComponent,
     DeleteCredentialDialogComponent,
+    EnableEncryptionDialogComponent,
   ],
   exports: [WebauthnLoginSettingsComponent],
 })
diff --git a/apps/web/src/locales/en/messages.json b/apps/web/src/locales/en/messages.json
index 0ec3b27cc38..4b423bd9556 100644
--- a/apps/web/src/locales/en/messages.json
+++ b/apps/web/src/locales/en/messages.json
@@ -674,8 +674,8 @@
   "encryptionNotSupported": {
     "message": "Encryption not supported"
   },
-  "encryptionNotEnabled": {
-    "message": "Encryption not enabled"
+  "enablePasskeyEncryption": {
+    "message": "Set up encryption"
   },
   "usedForEncryption": {
     "message": "Used for encryption"
diff --git a/libs/common/spec/fake-storage.service.ts b/libs/common/spec/fake-storage.service.ts
index ba3e4613466..7c9e5b32315 100644
--- a/libs/common/spec/fake-storage.service.ts
+++ b/libs/common/spec/fake-storage.service.ts
@@ -59,7 +59,7 @@ export class FakeStorageService implements AbstractStorageService {
     return Promise.resolve(this.store[key] != null);
   }
   save<T>(key: string, obj: T, options?: StorageOptions): Promise<void> {
-    this.mock.save(key, options);
+    this.mock.save(key, obj, options);
     this.store[key] = obj;
     this.updatesSubject.next({ key: key, updateType: "save" });
     return Promise.resolve();
diff --git a/libs/common/spec/utils.ts b/libs/common/spec/utils.ts
index 5053a71c874..ad5907f61d3 100644
--- a/libs/common/spec/utils.ts
+++ b/libs/common/spec/utils.ts
@@ -69,6 +69,10 @@ export function trackEmissions<T>(observable: Observable<T>): T[] {
       case "boolean":
         emissions.push(value);
         break;
+      case "symbol":
+        // Cheating types to make symbols work at all
+        emissions.push(value.toString() as T);
+        break;
       default: {
         emissions.push(clone(value));
       }
@@ -85,7 +89,7 @@ function clone(value: any): any {
   }
 }
 
-export async function awaitAsync(ms = 0) {
+export async function awaitAsync(ms = 1) {
   if (ms < 1) {
     await Promise.resolve();
   } else {
diff --git a/libs/common/src/platform/state/implementations/default-active-user-state.spec.ts b/libs/common/src/platform/state/implementations/default-active-user-state.spec.ts
index 065f7a8e959..64c1d1b233f 100644
--- a/libs/common/src/platform/state/implementations/default-active-user-state.spec.ts
+++ b/libs/common/src/platform/state/implementations/default-active-user-state.spec.ts
@@ -2,7 +2,7 @@
  * need to update test environment so trackEmissions works appropriately
  * @jest-environment ../shared/test.environment.ts
  */
-import { any, mock } from "jest-mock-extended";
+import { any, anySymbol, mock } from "jest-mock-extended";
 import { BehaviorSubject, firstValueFrom, of, timeout } from "rxjs";
 import { Jsonify } from "type-fest";
 
@@ -11,7 +11,7 @@ import { FakeStorageService } from "../../../../spec/fake-storage.service";
 import { AccountInfo, AccountService } from "../../../auth/abstractions/account.service";
 import { AuthenticationStatus } from "../../../auth/enums/authentication-status";
 import { UserId } from "../../../types/guid";
-import { KeyDefinition } from "../key-definition";
+import { KeyDefinition, userKeyBuilder } from "../key-definition";
 import { StateDefinition } from "../state-definition";
 
 import { DefaultActiveUserState } from "./default-active-user-state";
@@ -32,9 +32,10 @@ class TestState {
 }
 
 const testStateDefinition = new StateDefinition("fake", "disk");
-
+const cleanupDelayMs = 10;
 const testKeyDefinition = new KeyDefinition<TestState>(testStateDefinition, "fake", {
   deserializer: TestState.fromJSON,
+  cleanupDelayMs,
 });
 
 describe("DefaultActiveUserState", () => {
@@ -56,10 +57,14 @@ describe("DefaultActiveUserState", () => {
     );
   });
 
+  const makeUserId = (id: string) => {
+    return id != null ? (`00000000-0000-1000-a000-00000000000${id}` as UserId) : undefined;
+  };
+
   const changeActiveUser = async (id: string) => {
-    const userId = id != null ? `00000000-0000-1000-a000-00000000000${id}` : undefined;
+    const userId = makeUserId(id);
     activeAccountSubject.next({
-      id: userId as UserId,
+      id: userId,
       email: `test${id}@example.com`,
       name: `Test User ${id}`,
       status: AuthenticationStatus.Unlocked,
@@ -90,7 +95,7 @@ describe("DefaultActiveUserState", () => {
     const emissions = trackEmissions(userState.state$);
 
     // User signs in
-    changeActiveUser("1");
+    await changeActiveUser("1");
     await awaitAsync();
 
     // Service does an update
@@ -111,17 +116,17 @@ describe("DefaultActiveUserState", () => {
     expect(diskStorageService.mock.get).toHaveBeenNthCalledWith(
       1,
       "user_00000000-0000-1000-a000-000000000001_fake_fake",
-      any(),
+      any(), // options
     );
     expect(diskStorageService.mock.get).toHaveBeenNthCalledWith(
       2,
       "user_00000000-0000-1000-a000-000000000001_fake_fake",
-      any(),
+      any(), // options
     );
     expect(diskStorageService.mock.get).toHaveBeenNthCalledWith(
       3,
       "user_00000000-0000-1000-a000-000000000002_fake_fake",
-      any(),
+      any(), // options
     );
 
     // Should only have saved data for the first user
@@ -129,7 +134,8 @@ describe("DefaultActiveUserState", () => {
     expect(diskStorageService.mock.save).toHaveBeenNthCalledWith(
       1,
       "user_00000000-0000-1000-a000-000000000001_fake_fake",
-      any(),
+      updatedState,
+      any(), // options
     );
   });
 
@@ -183,15 +189,17 @@ describe("DefaultActiveUserState", () => {
   });
 
   it("should not emit a previous users value if that user is no longer active", async () => {
+    const user1Data: Jsonify<TestState> = {
+      date: "2020-09-21T13:14:17.648Z",
+      array: ["value"],
+    };
+    const user2Data: Jsonify<TestState> = {
+      date: "2020-09-21T13:14:17.648Z",
+      array: [],
+    };
     diskStorageService.internalUpdateStore({
-      "user_00000000-0000-1000-a000-000000000001_fake_fake": {
-        date: "2020-09-21T13:14:17.648Z",
-        array: ["value"],
-      } as Jsonify<TestState>,
-      "user_00000000-0000-1000-a000-000000000002_fake_fake": {
-        date: "2020-09-21T13:14:17.648Z",
-        array: [],
-      } as Jsonify<TestState>,
+      "user_00000000-0000-1000-a000-000000000001_fake_fake": user1Data,
+      "user_00000000-0000-1000-a000-000000000002_fake_fake": user2Data,
     });
 
     // This starts one subscription on the observable for tracking emissions throughout
@@ -203,7 +211,7 @@ describe("DefaultActiveUserState", () => {
 
     // This should always return a value right await
     const value = await firstValueFrom(userState.state$);
-    expect(value).toBeTruthy();
+    expect(value).toEqual(user1Data);
 
     // Make it such that there is no active user
     await changeActiveUser(undefined);
@@ -222,20 +230,34 @@ describe("DefaultActiveUserState", () => {
         rejectedError = err;
       });
 
-    expect(resolvedValue).toBeFalsy();
-    expect(rejectedError).toBeTruthy();
+    expect(resolvedValue).toBeUndefined();
+    expect(rejectedError).not.toBeUndefined();
     expect(rejectedError.message).toBe("Timeout has occurred");
 
     // We need to figure out if something should be emitted
     // when there becomes no active user, if we don't want that to emit
     // this value is correct.
-    expect(emissions).toHaveLength(2);
+    expect(emissions).toEqual([user1Data]);
+  });
+
+  it("should not emit twice if there are two listeners", async () => {
+    await changeActiveUser("1");
+    const emissions = trackEmissions(userState.state$);
+    const emissions2 = trackEmissions(userState.state$);
+    await awaitAsync();
+
+    expect(emissions).toEqual([
+      null, // Initial value
+    ]);
+    expect(emissions2).toEqual([
+      null, // Initial value
+    ]);
   });
 
   describe("update", () => {
     const newData = { date: new Date(), array: ["test"] };
     beforeEach(async () => {
-      changeActiveUser("1");
+      await changeActiveUser("1");
     });
 
     it("should save on update", async () => {
@@ -315,6 +337,8 @@ describe("DefaultActiveUserState", () => {
         return initialData;
       });
 
+      await awaitAsync();
+
       await userState.update((state, dependencies) => {
         expect(state).toEqual(initialData);
         return newData;
@@ -329,4 +353,303 @@ describe("DefaultActiveUserState", () => {
       ]);
     });
   });
+
+  describe("update races", () => {
+    const newData = { date: new Date(), array: ["test"] };
+    const userId = makeUserId("1");
+
+    beforeEach(async () => {
+      await changeActiveUser("1");
+      await awaitAsync();
+    });
+
+    test("subscriptions during an update should receive the current and latest", async () => {
+      const oldData = { date: new Date(2019, 1, 1), array: ["oldValue1"] };
+      await userState.update(() => {
+        return oldData;
+      });
+      const initialData = { date: new Date(2020, 1, 1), array: ["value1", "value2"] };
+      await userState.update(() => {
+        return initialData;
+      });
+
+      await awaitAsync();
+
+      const emissions = trackEmissions(userState.state$);
+      await awaitAsync();
+      expect(emissions).toEqual([initialData]);
+
+      let emissions2: TestState[];
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest.fn().mockImplementation(async (key: string, obj: any) => {
+        emissions2 = trackEmissions(userState.state$);
+        await originalSave(key, obj);
+      });
+
+      const val = await userState.update(() => {
+        return newData;
+      });
+
+      await awaitAsync(10);
+
+      expect(val).toEqual(newData);
+      expect(emissions).toEqual([initialData, newData]);
+      expect(emissions2).toEqual([initialData, newData]);
+    });
+
+    test("subscription during an aborted update should receive the last value", async () => {
+      // Seed with interesting data
+      const initialData = { date: new Date(2020, 1, 1), array: ["value1", "value2"] };
+      await userState.update(() => {
+        return initialData;
+      });
+
+      await awaitAsync();
+
+      const emissions = trackEmissions(userState.state$);
+      await awaitAsync();
+      expect(emissions).toEqual([initialData]);
+
+      let emissions2: TestState[];
+      const val = await userState.update(
+        (state) => {
+          return newData;
+        },
+        {
+          shouldUpdate: () => {
+            emissions2 = trackEmissions(userState.state$);
+            return false;
+          },
+        },
+      );
+
+      await awaitAsync();
+
+      expect(val).toEqual(initialData);
+      expect(emissions).toEqual([initialData]);
+
+      expect(emissions2).toEqual([initialData]);
+    });
+
+    test("updates should wait until previous update is complete", async () => {
+      trackEmissions(userState.state$);
+      await awaitAsync(); // storage updates are behind a promise
+
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest
+        .fn()
+        .mockImplementationOnce(async (key: string, obj: any) => {
+          let resolved = false;
+          await Promise.race([
+            userState.update(() => {
+              // deadlocks
+              resolved = true;
+              return newData;
+            }),
+            awaitAsync(100), // limit test to 100ms
+          ]);
+          expect(resolved).toBe(false);
+        })
+        .mockImplementation((...args) => {
+          return originalSave(...args);
+        });
+
+      await userState.update(() => {
+        return newData;
+      });
+    });
+
+    test("updates with FAKE_DEFAULT initial value should resolve correctly", async () => {
+      expect(userState["stateSubject"].value).toEqual(anySymbol()); // FAKE_DEFAULT
+      const val = await userState.update((state) => {
+        return newData;
+      });
+
+      expect(val).toEqual(newData);
+      const call = diskStorageService.mock.save.mock.calls[0];
+      expect(call[0]).toEqual(`user_${userId}_fake_fake`);
+      expect(call[1]).toEqual(newData);
+    });
+
+    it("does not await updates if the active user changes", async () => {
+      const initialUserId = (await firstValueFrom(accountService.activeAccount$)).id;
+      expect(initialUserId).toBe(userId);
+      trackEmissions(userState.state$);
+      await awaitAsync(); // storage updates are behind a promise
+
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest
+        .fn()
+        .mockImplementationOnce(async (key: string, obj: any) => {
+          let resolved = false;
+          await changeActiveUser("2");
+          await Promise.race([
+            userState.update(() => {
+              // should not deadlock because we updated the user
+              resolved = true;
+              return newData;
+            }),
+            awaitAsync(100), // limit test to 100ms
+          ]);
+          expect(resolved).toBe(true);
+        })
+        .mockImplementation((...args) => {
+          return originalSave(...args);
+        });
+
+      await userState.update(() => {
+        return newData;
+      });
+    });
+
+    it("stores updates for users in the correct place when active user changes mid-update", async () => {
+      trackEmissions(userState.state$);
+      await awaitAsync(); // storage updates are behind a promise
+
+      const user2Data = { date: new Date(), array: ["user 2 data"] };
+
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest
+        .fn()
+        .mockImplementationOnce(async (key: string, obj: any) => {
+          let resolved = false;
+          await changeActiveUser("2");
+          await Promise.race([
+            userState.update(() => {
+              // should not deadlock because we updated the user
+              resolved = true;
+              return user2Data;
+            }),
+            awaitAsync(100), // limit test to 100ms
+          ]);
+          expect(resolved).toBe(true);
+          await originalSave(key, obj);
+        })
+        .mockImplementation((...args) => {
+          return originalSave(...args);
+        });
+
+      await userState.update(() => {
+        return newData;
+      });
+      await awaitAsync();
+
+      expect(diskStorageService.mock.save).toHaveBeenCalledTimes(2);
+      const innerCall = diskStorageService.mock.save.mock.calls[0];
+      expect(innerCall[0]).toEqual(`user_${makeUserId("2")}_fake_fake`);
+      expect(innerCall[1]).toEqual(user2Data);
+      const outerCall = diskStorageService.mock.save.mock.calls[1];
+      expect(outerCall[0]).toEqual(`user_${makeUserId("1")}_fake_fake`);
+      expect(outerCall[1]).toEqual(newData);
+    });
+  });
+
+  describe("cleanup", () => {
+    const newData = { date: new Date(), array: ["test"] };
+    const userId = makeUserId("1");
+    let userKey: string;
+
+    beforeEach(async () => {
+      await changeActiveUser("1");
+      userKey = userKeyBuilder(userId, testKeyDefinition);
+    });
+
+    async function assertClean() {
+      const emissions = trackEmissions(userState["stateSubject"]);
+      const initial = structuredClone(emissions);
+
+      diskStorageService.save(userKey, newData);
+      await awaitAsync(); // storage updates are behind a promise
+
+      expect(emissions).toEqual(initial); // no longer listening to storage updates
+    }
+
+    it("should cleanup after last subscriber", async () => {
+      const subscription = userState.state$.subscribe();
+      await awaitAsync(); // storage updates are behind a promise
+
+      subscription.unsubscribe();
+      expect(userState["subscriberCount"].getValue()).toBe(0);
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      await assertClean();
+    });
+
+    it("should not cleanup if there are still subscribers", async () => {
+      const subscription1 = userState.state$.subscribe();
+      const sub2Emissions: TestState[] = [];
+      const subscription2 = userState.state$.subscribe((v) => sub2Emissions.push(v));
+      await awaitAsync(); // storage updates are behind a promise
+
+      subscription1.unsubscribe();
+
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      expect(userState["subscriberCount"].getValue()).toBe(1);
+
+      // Still be listening to storage updates
+      diskStorageService.save(userKey, newData);
+      await awaitAsync(); // storage updates are behind a promise
+      expect(sub2Emissions).toEqual([null, newData]);
+
+      subscription2.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      await assertClean();
+    });
+
+    it("can re-initialize after cleanup", async () => {
+      const subscription = userState.state$.subscribe();
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      const emissions = trackEmissions(userState.state$);
+      await awaitAsync();
+
+      diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      expect(emissions).toEqual([null, newData]);
+    });
+
+    it("should not cleanup if a subscriber joins during the cleanup delay", async () => {
+      const subscription = userState.state$.subscribe();
+      await awaitAsync();
+
+      await diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      expect(userState["subscriberCount"].getValue()).toBe(0);
+      // Do not wait long enough for cleanup
+      await awaitAsync(cleanupDelayMs / 2);
+
+      expect(userState["stateSubject"].value).toEqual(newData); // digging in to check that it hasn't been cleared
+      expect(userState["storageUpdateSubscription"]).not.toBeNull(); // still listening to storage updates
+    });
+
+    it("state$ observables are durable to cleanup", async () => {
+      const observable = userState.state$;
+      let subscription = observable.subscribe();
+
+      await diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      subscription = observable.subscribe();
+      await diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      expect(await firstValueFrom(observable)).toEqual(newData);
+    });
+  });
 });
diff --git a/libs/common/src/platform/state/implementations/default-active-user-state.ts b/libs/common/src/platform/state/implementations/default-active-user-state.ts
index 3d36af1d61c..02cd53cfb85 100644
--- a/libs/common/src/platform/state/implementations/default-active-user-state.ts
+++ b/libs/common/src/platform/state/implementations/default-active-user-state.ts
@@ -4,12 +4,12 @@ import {
   map,
   shareReplay,
   switchMap,
-  tap,
-  defer,
   firstValueFrom,
   combineLatestWith,
   filter,
   timeout,
+  Subscription,
+  tap,
 } from "rxjs";
 
 import { AccountService } from "../../../auth/abstractions/account.service";
@@ -31,13 +31,22 @@ const FAKE_DEFAULT = Symbol("fakeDefault");
 export class DefaultActiveUserState<T> implements ActiveUserState<T> {
   [activeMarker]: true;
   private formattedKey$: Observable<string>;
+  private updatePromise: Promise<T> | null = null;
+  private storageUpdateSubscription: Subscription;
+  private activeAccountUpdateSubscription: Subscription;
+  private subscriberCount = new BehaviorSubject<number>(0);
+  private stateObservable: Observable<T>;
+  private reinitialize = false;
 
   protected stateSubject: BehaviorSubject<T | typeof FAKE_DEFAULT> = new BehaviorSubject<
     T | typeof FAKE_DEFAULT
   >(FAKE_DEFAULT);
   private stateSubject$ = this.stateSubject.asObservable();
 
-  state$: Observable<T>;
+  get state$() {
+    this.stateObservable = this.stateObservable ?? this.initializeObservable();
+    return this.stateObservable;
+  }
 
   constructor(
     protected keyDefinition: KeyDefinition<T>,
@@ -51,62 +60,12 @@ export class DefaultActiveUserState<T> implements ActiveUserState<T> {
           ? userKeyBuilder(account.id, this.keyDefinition)
           : null,
       ),
+      tap(() => {
+        // We have a new key, so we should forget about previous update promises
+        this.updatePromise = null;
+      }),
       shareReplay({ bufferSize: 1, refCount: false }),
     );
-
-    const activeAccountData$ = this.formattedKey$.pipe(
-      switchMap(async (key) => {
-        if (key == null) {
-          return FAKE_DEFAULT;
-        }
-        return await getStoredValue(
-          key,
-          this.chosenStorageLocation,
-          this.keyDefinition.deserializer,
-        );
-      }),
-      // Share the execution
-      shareReplay({ refCount: false, bufferSize: 1 }),
-    );
-
-    const storageUpdates$ = this.chosenStorageLocation.updates$.pipe(
-      combineLatestWith(this.formattedKey$),
-      filter(([update, key]) => key !== null && update.key === key),
-      switchMap(async ([update, key]) => {
-        if (update.updateType === "remove") {
-          return null;
-        }
-        const data = await getStoredValue(
-          key,
-          this.chosenStorageLocation,
-          this.keyDefinition.deserializer,
-        );
-        return data;
-      }),
-    );
-
-    // Whomever subscribes to this data, should be notified of updated data
-    // if someone calls my update() method, or the active user changes.
-    this.state$ = defer(() => {
-      const accountChangeSubscription = activeAccountData$.subscribe((data) => {
-        this.stateSubject.next(data);
-      });
-      const storageUpdateSubscription = storageUpdates$.subscribe((data) => {
-        this.stateSubject.next(data);
-      });
-
-      return this.stateSubject$.pipe(
-        tap({
-          complete: () => {
-            accountChangeSubscription.unsubscribe();
-            storageUpdateSubscription.unsubscribe();
-          },
-        }),
-      );
-    })
-      // I fake the generic here because I am filtering out the other union type
-      // and this makes it so that typescript understands the true type
-      .pipe(filter<T>((value) => value != FAKE_DEFAULT));
   }
 
   async update<TCombine>(
@@ -114,8 +73,34 @@ export class DefaultActiveUserState<T> implements ActiveUserState<T> {
     options: StateUpdateOptions<T, TCombine> = {},
   ): Promise<T> {
     options = populateOptionsWithDefault(options);
+    try {
+      if (this.updatePromise != null) {
+        await this.updatePromise;
+      }
+      this.updatePromise = this.internalUpdate(configureState, options);
+      const newState = await this.updatePromise;
+      return newState;
+    } finally {
+      this.updatePromise = null;
+    }
+  }
+
+  // TODO: this should be removed
+  async getFromState(): Promise<T> {
     const key = await this.createKey();
-    const currentState = await this.getGuaranteedState(key);
+    return await getStoredValue(key, this.chosenStorageLocation, this.keyDefinition.deserializer);
+  }
+
+  createDerived<TTo>(converter: Converter<T, TTo>): DerivedUserState<TTo> {
+    return new DefaultDerivedUserState<T, TTo>(converter, this.encryptService, this);
+  }
+
+  private async internalUpdate<TCombine>(
+    configureState: (state: T, dependency: TCombine) => T,
+    options: StateUpdateOptions<T, TCombine>,
+  ) {
+    const key = await this.createKey();
+    const currentState = await this.getStateForUpdate(key);
     const combinedDependencies =
       options.combineLatestWith != null
         ? await firstValueFrom(options.combineLatestWith.pipe(timeout(options.msTimeout)))
@@ -130,13 +115,59 @@ export class DefaultActiveUserState<T> implements ActiveUserState<T> {
     return newState;
   }
 
-  async getFromState(): Promise<T> {
-    const key = await this.createKey();
-    return await getStoredValue(key, this.chosenStorageLocation, this.keyDefinition.deserializer);
-  }
+  private initializeObservable() {
+    this.storageUpdateSubscription = this.chosenStorageLocation.updates$
+      .pipe(
+        combineLatestWith(this.formattedKey$),
+        filter(([update, key]) => key !== null && update.key === key),
+        switchMap(async ([update, key]) => {
+          if (update.updateType === "remove") {
+            return null;
+          }
+          return await this.getState(key);
+        }),
+      )
+      .subscribe((v) => this.stateSubject.next(v));
 
-  createDerived<TTo>(converter: Converter<T, TTo>): DerivedUserState<TTo> {
-    return new DefaultDerivedUserState<T, TTo>(converter, this.encryptService, this);
+    this.activeAccountUpdateSubscription = this.formattedKey$
+      .pipe(
+        switchMap(async (key) => {
+          if (key == null) {
+            return FAKE_DEFAULT;
+          }
+          return await this.getState(key);
+        }),
+      )
+      .subscribe((v) => this.stateSubject.next(v));
+
+    this.subscriberCount.subscribe((count) => {
+      if (count === 0 && this.stateObservable != null) {
+        this.triggerCleanup();
+      }
+    });
+
+    return new Observable<T>((subscriber) => {
+      this.incrementSubscribers();
+
+      // reinitialize listeners after cleanup
+      if (this.reinitialize) {
+        this.reinitialize = false;
+        this.initializeObservable();
+      }
+
+      const prevUnsubscribe = subscriber.unsubscribe.bind(subscriber);
+      subscriber.unsubscribe = () => {
+        this.decrementSubscribers();
+        prevUnsubscribe();
+      };
+
+      return this.stateSubject
+        .pipe(
+          // Filter out fake default, which is used to indicate that state is not ready to be emitted yet.
+          filter((i) => i !== FAKE_DEFAULT),
+        )
+        .subscribe(subscriber);
+    });
   }
 
   protected async createKey(): Promise<string> {
@@ -147,22 +178,47 @@ export class DefaultActiveUserState<T> implements ActiveUserState<T> {
     return formattedKey;
   }
 
-  protected async getGuaranteedState(key: string) {
+  /** For use in update methods, does not wait for update to complete before yielding state.
+   * The expectation is that that await is already done
+   */
+  protected async getStateForUpdate(key: string) {
     const currentValue = this.stateSubject.getValue();
-    return currentValue === FAKE_DEFAULT ? await this.seedInitial(key) : currentValue;
+    return currentValue === FAKE_DEFAULT
+      ? await getStoredValue(key, this.chosenStorageLocation, this.keyDefinition.deserializer)
+      : currentValue;
   }
 
-  private async seedInitial(key: string): Promise<T> {
-    const value = await getStoredValue(
-      key,
-      this.chosenStorageLocation,
-      this.keyDefinition.deserializer,
-    );
-    this.stateSubject.next(value);
-    return value;
+  /** To be used in observables. Awaits updates to ensure they are complete */
+  private async getState(key: string): Promise<T> {
+    if (this.updatePromise != null) {
+      await this.updatePromise;
+    }
+    return await getStoredValue(key, this.chosenStorageLocation, this.keyDefinition.deserializer);
   }
 
   protected saveToStorage(key: string, data: T): Promise<void> {
     return this.chosenStorageLocation.save(key, data);
   }
+
+  private incrementSubscribers() {
+    this.subscriberCount.next(this.subscriberCount.value + 1);
+  }
+
+  private decrementSubscribers() {
+    this.subscriberCount.next(this.subscriberCount.value - 1);
+  }
+
+  private triggerCleanup() {
+    setTimeout(() => {
+      if (this.subscriberCount.value === 0) {
+        this.updatePromise = null;
+        this.storageUpdateSubscription?.unsubscribe();
+        this.activeAccountUpdateSubscription?.unsubscribe();
+        this.subscriberCount.complete();
+        this.subscriberCount = new BehaviorSubject<number>(0);
+        this.stateSubject.next(FAKE_DEFAULT);
+        this.reinitialize = true;
+      }
+    }, this.keyDefinition.cleanupDelayMs);
+  }
 }
diff --git a/libs/common/src/platform/state/implementations/default-global-state.spec.ts b/libs/common/src/platform/state/implementations/default-global-state.spec.ts
index ae6cd1adbfd..35ce0fa0983 100644
--- a/libs/common/src/platform/state/implementations/default-global-state.spec.ts
+++ b/libs/common/src/platform/state/implementations/default-global-state.spec.ts
@@ -3,6 +3,7 @@
  * @jest-environment ../shared/test.environment.ts
  */
 
+import { anySymbol } from "jest-mock-extended";
 import { firstValueFrom, of } from "rxjs";
 import { Jsonify } from "type-fest";
 
@@ -28,9 +29,10 @@ class TestState {
 }
 
 const testStateDefinition = new StateDefinition("fake", "disk");
-
+const cleanupDelayMs = 10;
 const testKeyDefinition = new KeyDefinition<TestState>(testStateDefinition, "fake", {
   deserializer: TestState.fromJSON,
+  cleanupDelayMs,
 });
 const globalKey = globalKeyBuilder(testKeyDefinition);
 
@@ -79,6 +81,19 @@ describe("DefaultGlobalState", () => {
       expect(diskStorageService.mock.get).toHaveBeenCalledWith("global_fake_fake", undefined);
       expect(state).toBeTruthy();
     });
+
+    it("should not emit twice if there are two listeners", async () => {
+      const emissions = trackEmissions(globalState.state$);
+      const emissions2 = trackEmissions(globalState.state$);
+      await awaitAsync();
+
+      expect(emissions).toEqual([
+        null, // Initial value
+      ]);
+      expect(emissions2).toEqual([
+        null, // Initial value
+      ]);
+    });
   });
 
   describe("update", () => {
@@ -133,6 +148,7 @@ describe("DefaultGlobalState", () => {
 
     it("should not update if shouldUpdate returns false", async () => {
       const emissions = trackEmissions(globalState.state$);
+      await awaitAsync(); // storage updates are behind a promise
 
       const result = await globalState.update(
         (state) => {
@@ -198,4 +214,212 @@ describe("DefaultGlobalState", () => {
       expect(emissions).toEqual(expect.arrayContaining([initialState, newState]));
     });
   });
+
+  describe("update races", () => {
+    test("subscriptions during an update should receive the current and  latest data", async () => {
+      const oldData = { date: new Date(2019, 1, 1) };
+      await globalState.update(() => {
+        return oldData;
+      });
+      const initialData = { date: new Date(2020, 1, 1) };
+      await globalState.update(() => {
+        return initialData;
+      });
+
+      await awaitAsync();
+
+      const emissions = trackEmissions(globalState.state$);
+      await awaitAsync();
+      expect(emissions).toEqual([initialData]);
+
+      let emissions2: TestState[];
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest.fn().mockImplementation(async (key: string, obj: any) => {
+        emissions2 = trackEmissions(globalState.state$);
+        await originalSave(key, obj);
+      });
+
+      const val = await globalState.update(() => {
+        return newData;
+      });
+
+      await awaitAsync(10);
+
+      expect(val).toEqual(newData);
+      expect(emissions).toEqual([initialData, newData]);
+      expect(emissions2).toEqual([initialData, newData]);
+    });
+
+    test("subscription during an aborted update should receive the last value", async () => {
+      // Seed with interesting data
+      const initialData = { date: new Date(2020, 1, 1) };
+      await globalState.update(() => {
+        return initialData;
+      });
+
+      await awaitAsync();
+
+      const emissions = trackEmissions(globalState.state$);
+      await awaitAsync();
+      expect(emissions).toEqual([initialData]);
+
+      let emissions2: TestState[];
+      const val = await globalState.update(
+        () => {
+          return newData;
+        },
+        {
+          shouldUpdate: () => {
+            emissions2 = trackEmissions(globalState.state$);
+            return false;
+          },
+        },
+      );
+
+      await awaitAsync();
+
+      expect(val).toEqual(initialData);
+      expect(emissions).toEqual([initialData]);
+
+      expect(emissions2).toEqual([initialData]);
+    });
+
+    test("updates should wait until previous update is complete", async () => {
+      trackEmissions(globalState.state$);
+      await awaitAsync(); // storage updates are behind a promise
+
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest
+        .fn()
+        .mockImplementationOnce(async () => {
+          let resolved = false;
+          await Promise.race([
+            globalState.update(() => {
+              // deadlocks
+              resolved = true;
+              return newData;
+            }),
+            awaitAsync(100), // limit test to 100ms
+          ]);
+          expect(resolved).toBe(false);
+        })
+        .mockImplementation(originalSave);
+
+      await globalState.update((state) => {
+        return newData;
+      });
+    });
+
+    test("updates with FAKE_DEFAULT initial value should resolve correctly", async () => {
+      expect(globalState["stateSubject"].value).toEqual(anySymbol()); // FAKE_DEFAULT
+      const val = await globalState.update((state) => {
+        return newData;
+      });
+
+      expect(val).toEqual(newData);
+      const call = diskStorageService.mock.save.mock.calls[0];
+      expect(call[0]).toEqual("global_fake_fake");
+      expect(call[1]).toEqual(newData);
+    });
+  });
+
+  describe("cleanup", () => {
+    async function assertClean() {
+      const emissions = trackEmissions(globalState["stateSubject"]);
+      const initial = structuredClone(emissions);
+
+      diskStorageService.save(globalKey, newData);
+      await awaitAsync(); // storage updates are behind a promise
+
+      expect(emissions).toEqual(initial); // no longer listening to storage updates
+    }
+
+    it("should cleanup after last subscriber", async () => {
+      const subscription = globalState.state$.subscribe();
+      await awaitAsync(); // storage updates are behind a promise
+
+      subscription.unsubscribe();
+      expect(globalState["subscriberCount"].getValue()).toBe(0);
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      await assertClean();
+    });
+
+    it("should not cleanup if there are still subscribers", async () => {
+      const subscription1 = globalState.state$.subscribe();
+      const sub2Emissions: TestState[] = [];
+      const subscription2 = globalState.state$.subscribe((v) => sub2Emissions.push(v));
+      await awaitAsync(); // storage updates are behind a promise
+
+      subscription1.unsubscribe();
+
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      expect(globalState["subscriberCount"].getValue()).toBe(1);
+
+      // Still be listening to storage updates
+      diskStorageService.save(globalKey, newData);
+      await awaitAsync(); // storage updates are behind a promise
+      expect(sub2Emissions).toEqual([null, newData]);
+
+      subscription2.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      await assertClean();
+    });
+
+    it("can re-initialize after cleanup", async () => {
+      const subscription = globalState.state$.subscribe();
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      const emissions = trackEmissions(globalState.state$);
+      await awaitAsync();
+
+      diskStorageService.save(globalKey, newData);
+      await awaitAsync();
+
+      expect(emissions).toEqual([null, newData]);
+    });
+
+    it("should not cleanup if a subscriber joins during the cleanup delay", async () => {
+      const subscription = globalState.state$.subscribe();
+      await awaitAsync();
+
+      await diskStorageService.save(globalKey, newData);
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      expect(globalState["subscriberCount"].getValue()).toBe(0);
+      // Do not wait long enough for cleanup
+      await awaitAsync(cleanupDelayMs / 2);
+
+      expect(globalState["stateSubject"].value).toEqual(newData); // digging in to check that it hasn't been cleared
+      expect(globalState["storageUpdateSubscription"]).not.toBeNull(); // still listening to storage updates
+    });
+
+    it("state$ observables are durable to cleanup", async () => {
+      const observable = globalState.state$;
+      let subscription = observable.subscribe();
+
+      await diskStorageService.save(globalKey, newData);
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      subscription = observable.subscribe();
+      await diskStorageService.save(globalKey, newData);
+      await awaitAsync();
+
+      expect(await firstValueFrom(observable)).toEqual(newData);
+    });
+  });
 });
diff --git a/libs/common/src/platform/state/implementations/default-global-state.ts b/libs/common/src/platform/state/implementations/default-global-state.ts
index 8e08717f721..73a3fe5d046 100644
--- a/libs/common/src/platform/state/implementations/default-global-state.ts
+++ b/libs/common/src/platform/state/implementations/default-global-state.ts
@@ -1,12 +1,10 @@
 import {
   BehaviorSubject,
   Observable,
-  defer,
+  Subscription,
   filter,
   firstValueFrom,
-  shareReplay,
   switchMap,
-  tap,
   timeout,
 } from "rxjs";
 
@@ -23,54 +21,26 @@ const FAKE_DEFAULT = Symbol("fakeDefault");
 
 export class DefaultGlobalState<T> implements GlobalState<T> {
   private storageKey: string;
+  private updatePromise: Promise<T> | null = null;
+  private storageUpdateSubscription: Subscription;
+  private subscriberCount = new BehaviorSubject<number>(0);
+  private stateObservable: Observable<T>;
+  private reinitialize = false;
 
   protected stateSubject: BehaviorSubject<T | typeof FAKE_DEFAULT> = new BehaviorSubject<
     T | typeof FAKE_DEFAULT
   >(FAKE_DEFAULT);
 
-  state$: Observable<T>;
+  get state$() {
+    this.stateObservable = this.stateObservable ?? this.initializeObservable();
+    return this.stateObservable;
+  }
 
   constructor(
     private keyDefinition: KeyDefinition<T>,
     private chosenLocation: AbstractStorageService & ObservableStorageService,
   ) {
     this.storageKey = globalKeyBuilder(this.keyDefinition);
-
-    const storageUpdates$ = this.chosenLocation.updates$.pipe(
-      filter((update) => update.key === this.storageKey),
-      switchMap(async (update) => {
-        if (update.updateType === "remove") {
-          return null;
-        }
-        return await getStoredValue(
-          this.storageKey,
-          this.chosenLocation,
-          this.keyDefinition.deserializer,
-        );
-      }),
-      shareReplay({ bufferSize: 1, refCount: false }),
-    );
-
-    this.state$ = defer(() => {
-      const storageUpdateSubscription = storageUpdates$.subscribe((value) => {
-        this.stateSubject.next(value);
-      });
-
-      this.getFromState().then((s) => {
-        this.stateSubject.next(s);
-      });
-
-      return this.stateSubject.pipe(
-        tap({
-          complete: () => {
-            storageUpdateSubscription.unsubscribe();
-          },
-        }),
-      );
-    }).pipe(
-      shareReplay({ refCount: false, bufferSize: 1 }),
-      filter<T>((i) => i != FAKE_DEFAULT),
-    );
   }
 
   async update<TCombine>(
@@ -78,7 +48,24 @@ export class DefaultGlobalState<T> implements GlobalState<T> {
     options: StateUpdateOptions<T, TCombine> = {},
   ): Promise<T> {
     options = populateOptionsWithDefault(options);
-    const currentState = await this.getGuaranteedState();
+    if (this.updatePromise != null) {
+      await this.updatePromise;
+    }
+
+    try {
+      this.updatePromise = this.internalUpdate(configureState, options);
+      const newState = await this.updatePromise;
+      return newState;
+    } finally {
+      this.updatePromise = null;
+    }
+  }
+
+  private async internalUpdate<TCombine>(
+    configureState: (state: T, dependency: TCombine) => T,
+    options: StateUpdateOptions<T, TCombine>,
+  ): Promise<T> {
+    const currentState = await this.getStateForUpdate();
     const combinedDependencies =
       options.combineLatestWith != null
         ? await firstValueFrom(options.combineLatestWith.pipe(timeout(options.msTimeout)))
@@ -93,16 +80,94 @@ export class DefaultGlobalState<T> implements GlobalState<T> {
     return newState;
   }
 
-  private async getGuaranteedState() {
+  private initializeObservable() {
+    this.storageUpdateSubscription = this.chosenLocation.updates$
+      .pipe(
+        filter((update) => update.key === this.storageKey),
+        switchMap(async (update) => {
+          if (update.updateType === "remove") {
+            return null;
+          }
+          return await this.getFromState();
+        }),
+      )
+      .subscribe((v) => this.stateSubject.next(v));
+
+    this.subscriberCount.subscribe((count) => {
+      if (count === 0 && this.stateObservable != null) {
+        this.triggerCleanup();
+      }
+    });
+
+    // Intentionally un-awaited promise, we don't want to delay return of observable, but we do want to
+    // trigger populating it immediately.
+    this.getFromState().then((s) => {
+      this.stateSubject.next(s);
+    });
+
+    return new Observable<T>((subscriber) => {
+      this.incrementSubscribers();
+
+      // reinitialize listeners after cleanup
+      if (this.reinitialize) {
+        this.reinitialize = false;
+        this.initializeObservable();
+      }
+
+      const prevUnsubscribe = subscriber.unsubscribe.bind(subscriber);
+      subscriber.unsubscribe = () => {
+        this.decrementSubscribers();
+        prevUnsubscribe();
+      };
+
+      return this.stateSubject
+        .pipe(
+          // Filter out fake default, which is used to indicate that state is not ready to be emitted yet.
+          filter<T>((i) => i != FAKE_DEFAULT),
+        )
+        .subscribe(subscriber);
+    });
+  }
+
+  /** For use in update methods, does not wait for update to complete before yielding state.
+   * The expectation is that that await is already done
+   */
+  private async getStateForUpdate() {
     const currentValue = this.stateSubject.getValue();
-    return currentValue === FAKE_DEFAULT ? await this.getFromState() : currentValue;
+    return currentValue === FAKE_DEFAULT
+      ? await getStoredValue(this.storageKey, this.chosenLocation, this.keyDefinition.deserializer)
+      : currentValue;
   }
 
   async getFromState(): Promise<T> {
+    if (this.updatePromise != null) {
+      return await this.updatePromise;
+    }
     return await getStoredValue(
       this.storageKey,
       this.chosenLocation,
       this.keyDefinition.deserializer,
     );
   }
+
+  private incrementSubscribers() {
+    this.subscriberCount.next(this.subscriberCount.value + 1);
+  }
+
+  private decrementSubscribers() {
+    this.subscriberCount.next(this.subscriberCount.value - 1);
+  }
+
+  private triggerCleanup() {
+    setTimeout(() => {
+      if (this.subscriberCount.value === 0) {
+        this.updatePromise = null;
+        this.storageUpdateSubscription.unsubscribe();
+        this.subscriberCount.complete();
+        this.subscriberCount = new BehaviorSubject<number>(0);
+        this.stateSubject.next(FAKE_DEFAULT);
+        this.reinitialize = true;
+      }
+    }, this.keyDefinition.cleanupDelayMs);
+  }
 }
diff --git a/libs/common/src/platform/state/implementations/default-single-user-state.spec.ts b/libs/common/src/platform/state/implementations/default-single-user-state.spec.ts
index a25ee863e6b..715b770b2ae 100644
--- a/libs/common/src/platform/state/implementations/default-single-user-state.spec.ts
+++ b/libs/common/src/platform/state/implementations/default-single-user-state.spec.ts
@@ -3,6 +3,7 @@
  * @jest-environment ../shared/test.environment.ts
  */
 
+import { anySymbol } from "jest-mock-extended";
 import { firstValueFrom, of } from "rxjs";
 import { Jsonify } from "type-fest";
 
@@ -30,21 +31,22 @@ class TestState {
 }
 
 const testStateDefinition = new StateDefinition("fake", "disk");
-
+const cleanupDelayMs = 10;
 const testKeyDefinition = new KeyDefinition<TestState>(testStateDefinition, "fake", {
   deserializer: TestState.fromJSON,
+  cleanupDelayMs,
 });
 const userId = Utils.newGuid() as UserId;
 const userKey = userKeyBuilder(userId, testKeyDefinition);
 
 describe("DefaultSingleUserState", () => {
   let diskStorageService: FakeStorageService;
-  let globalState: DefaultSingleUserState<TestState>;
+  let userState: DefaultSingleUserState<TestState>;
   const newData = { date: new Date() };
 
   beforeEach(() => {
     diskStorageService = new FakeStorageService();
-    globalState = new DefaultSingleUserState(
+    userState = new DefaultSingleUserState(
       userId,
       testKeyDefinition,
       null, // Not testing anything with encrypt service
@@ -58,7 +60,7 @@ describe("DefaultSingleUserState", () => {
 
   describe("state$", () => {
     it("should emit when storage updates", async () => {
-      const emissions = trackEmissions(globalState.state$);
+      const emissions = trackEmissions(userState.state$);
       await diskStorageService.save(userKey, newData);
       await awaitAsync();
 
@@ -69,7 +71,7 @@ describe("DefaultSingleUserState", () => {
     });
 
     it("should not emit when update key does not match", async () => {
-      const emissions = trackEmissions(globalState.state$);
+      const emissions = trackEmissions(userState.state$);
       await diskStorageService.save("wrong_key", newData);
 
       expect(emissions).toHaveLength(0);
@@ -82,7 +84,7 @@ describe("DefaultSingleUserState", () => {
       });
       diskStorageService.internalUpdateStore(initialStorage);
 
-      const state = await firstValueFrom(globalState.state$);
+      const state = await firstValueFrom(userState.state$);
       expect(diskStorageService.mock.get).toHaveBeenCalledTimes(1);
       expect(diskStorageService.mock.get).toHaveBeenCalledWith(
         `user_${userId}_fake_fake`,
@@ -94,7 +96,7 @@ describe("DefaultSingleUserState", () => {
 
   describe("update", () => {
     it("should save on update", async () => {
-      const result = await globalState.update((state) => {
+      const result = await userState.update((state) => {
         return newData;
       });
 
@@ -103,10 +105,10 @@ describe("DefaultSingleUserState", () => {
     });
 
     it("should emit once per update", async () => {
-      const emissions = trackEmissions(globalState.state$);
+      const emissions = trackEmissions(userState.state$);
       await awaitAsync(); // storage updates are behind a promise
 
-      await globalState.update((state) => {
+      await userState.update((state) => {
         return newData;
       });
 
@@ -119,12 +121,12 @@ describe("DefaultSingleUserState", () => {
     });
 
     it("should provided combined dependencies", async () => {
-      const emissions = trackEmissions(globalState.state$);
+      const emissions = trackEmissions(userState.state$);
       await awaitAsync(); // storage updates are behind a promise
 
       const combinedDependencies = { date: new Date() };
 
-      await globalState.update(
+      await userState.update(
         (state, dependencies) => {
           expect(dependencies).toEqual(combinedDependencies);
           return newData;
@@ -143,9 +145,10 @@ describe("DefaultSingleUserState", () => {
     });
 
     it("should not update if shouldUpdate returns false", async () => {
-      const emissions = trackEmissions(globalState.state$);
+      const emissions = trackEmissions(userState.state$);
+      await awaitAsync(); // storage updates are behind a promise
 
-      const result = await globalState.update(
+      const result = await userState.update(
         (state) => {
           return newData;
         },
@@ -160,18 +163,18 @@ describe("DefaultSingleUserState", () => {
     });
 
     it("should provide the update callback with the current State", async () => {
-      const emissions = trackEmissions(globalState.state$);
+      const emissions = trackEmissions(userState.state$);
       await awaitAsync(); // storage updates are behind a promise
 
       // Seed with interesting data
       const initialData = { date: new Date(2020, 1, 1) };
-      await globalState.update((state, dependencies) => {
+      await userState.update((state, dependencies) => {
         return initialData;
       });
 
       await awaitAsync();
 
-      await globalState.update((state) => {
+      await userState.update((state) => {
         expect(state).toEqual(initialData);
         return newData;
       });
@@ -193,14 +196,14 @@ describe("DefaultSingleUserState", () => {
       initialStorage[userKey] = initialState;
       diskStorageService.internalUpdateStore(initialStorage);
 
-      const emissions = trackEmissions(globalState.state$);
+      const emissions = trackEmissions(userState.state$);
       await awaitAsync(); // storage updates are behind a promise
 
       const newState = {
         ...initialState,
         date: new Date(initialState.date.getFullYear(), initialState.date.getMonth() + 1),
       };
-      const actual = await globalState.update((existingState) => newState);
+      const actual = await userState.update((existingState) => newState);
 
       await awaitAsync();
 
@@ -209,4 +212,212 @@ describe("DefaultSingleUserState", () => {
       expect(emissions).toEqual(expect.arrayContaining([initialState, newState]));
     });
   });
+
+  describe("update races", () => {
+    test("subscriptions during an update should receive the current and latest data", async () => {
+      const oldData = { date: new Date(2019, 1, 1) };
+      await userState.update(() => {
+        return oldData;
+      });
+      const initialData = { date: new Date(2020, 1, 1) };
+      await userState.update(() => {
+        return initialData;
+      });
+
+      await awaitAsync();
+
+      const emissions = trackEmissions(userState.state$);
+      await awaitAsync();
+      expect(emissions).toEqual([initialData]);
+
+      let emissions2: TestState[];
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest.fn().mockImplementation(async (key: string, obj: any) => {
+        emissions2 = trackEmissions(userState.state$);
+        await originalSave(key, obj);
+      });
+
+      const val = await userState.update(() => {
+        return newData;
+      });
+
+      await awaitAsync(10);
+
+      expect(val).toEqual(newData);
+      expect(emissions).toEqual([initialData, newData]);
+      expect(emissions2).toEqual([initialData, newData]);
+    });
+
+    test("subscription during an aborted update should receive the last value", async () => {
+      // Seed with interesting data
+      const initialData = { date: new Date(2020, 1, 1) };
+      await userState.update(() => {
+        return initialData;
+      });
+
+      await awaitAsync();
+
+      const emissions = trackEmissions(userState.state$);
+      await awaitAsync();
+      expect(emissions).toEqual([initialData]);
+
+      let emissions2: TestState[];
+      const val = await userState.update(
+        (state) => {
+          return newData;
+        },
+        {
+          shouldUpdate: () => {
+            emissions2 = trackEmissions(userState.state$);
+            return false;
+          },
+        },
+      );
+
+      await awaitAsync();
+
+      expect(val).toEqual(initialData);
+      expect(emissions).toEqual([initialData]);
+
+      expect(emissions2).toEqual([initialData]);
+    });
+
+    test("updates should wait until previous update is complete", async () => {
+      trackEmissions(userState.state$);
+      await awaitAsync(); // storage updates are behind a promise
+
+      const originalSave = diskStorageService.save.bind(diskStorageService);
+      diskStorageService.save = jest
+        .fn()
+        .mockImplementationOnce(async () => {
+          let resolved = false;
+          await Promise.race([
+            userState.update(() => {
+              // deadlocks
+              resolved = true;
+              return newData;
+            }),
+            awaitAsync(100), // limit test to 100ms
+          ]);
+          expect(resolved).toBe(false);
+        })
+        .mockImplementation(originalSave);
+
+      await userState.update((state) => {
+        return newData;
+      });
+    });
+
+    test("updates with FAKE_DEFAULT initial value should resolve correctly", async () => {
+      expect(userState["stateSubject"].value).toEqual(anySymbol()); // FAKE_DEFAULT
+      const val = await userState.update((state) => {
+        return newData;
+      });
+
+      expect(val).toEqual(newData);
+      const call = diskStorageService.mock.save.mock.calls[0];
+      expect(call[0]).toEqual(`user_${userId}_fake_fake`);
+      expect(call[1]).toEqual(newData);
+    });
+  });
+
+  describe("cleanup", () => {
+    async function assertClean() {
+      const emissions = trackEmissions(userState["stateSubject"]);
+      const initial = structuredClone(emissions);
+
+      diskStorageService.save(userKey, newData);
+      await awaitAsync(); // storage updates are behind a promise
+
+      expect(emissions).toEqual(initial); // no longer listening to storage updates
+    }
+
+    it("should cleanup after last subscriber", async () => {
+      const subscription = userState.state$.subscribe();
+      await awaitAsync(); // storage updates are behind a promise
+
+      subscription.unsubscribe();
+      expect(userState["subscriberCount"].getValue()).toBe(0);
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      await assertClean();
+    });
+
+    it("should not cleanup if there are still subscribers", async () => {
+      const subscription1 = userState.state$.subscribe();
+      const sub2Emissions: TestState[] = [];
+      const subscription2 = userState.state$.subscribe((v) => sub2Emissions.push(v));
+      await awaitAsync(); // storage updates are behind a promise
+
+      subscription1.unsubscribe();
+
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      expect(userState["subscriberCount"].getValue()).toBe(1);
+
+      // Still be listening to storage updates
+      diskStorageService.save(userKey, newData);
+      await awaitAsync(); // storage updates are behind a promise
+      expect(sub2Emissions).toEqual([null, newData]);
+
+      subscription2.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      await assertClean();
+    });
+
+    it("can re-initialize after cleanup", async () => {
+      const subscription = userState.state$.subscribe();
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      const emissions = trackEmissions(userState.state$);
+      await awaitAsync();
+
+      diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      expect(emissions).toEqual([null, newData]);
+    });
+
+    it("should not cleanup if a subscriber joins during the cleanup delay", async () => {
+      const subscription = userState.state$.subscribe();
+      await awaitAsync();
+
+      await diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      expect(userState["subscriberCount"].getValue()).toBe(0);
+      // Do not wait long enough for cleanup
+      await awaitAsync(cleanupDelayMs / 2);
+
+      expect(userState["stateSubject"].value).toEqual(newData); // digging in to check that it hasn't been cleared
+      expect(userState["storageUpdateSubscription"]).not.toBeNull(); // still listening to storage updates
+    });
+
+    it("state$ observables are durable to cleanup", async () => {
+      const observable = userState.state$;
+      let subscription = observable.subscribe();
+
+      await diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      subscription.unsubscribe();
+      // Wait for cleanup
+      await awaitAsync(cleanupDelayMs * 2);
+
+      subscription = observable.subscribe();
+      await diskStorageService.save(userKey, newData);
+      await awaitAsync();
+
+      expect(await firstValueFrom(observable)).toEqual(newData);
+    });
+  });
 });
diff --git a/libs/common/src/platform/state/implementations/default-single-user-state.ts b/libs/common/src/platform/state/implementations/default-single-user-state.ts
index 46fa00ffb35..4c7c70d4267 100644
--- a/libs/common/src/platform/state/implementations/default-single-user-state.ts
+++ b/libs/common/src/platform/state/implementations/default-single-user-state.ts
@@ -1,12 +1,10 @@
 import {
   BehaviorSubject,
   Observable,
-  defer,
+  Subscription,
   filter,
   firstValueFrom,
-  shareReplay,
   switchMap,
-  tap,
   timeout,
 } from "rxjs";
 
@@ -23,16 +21,25 @@ import { Converter, SingleUserState } from "../user-state";
 
 import { DefaultDerivedUserState } from "./default-derived-state";
 import { getStoredValue } from "./util";
+
 const FAKE_DEFAULT = Symbol("fakeDefault");
 
 export class DefaultSingleUserState<T> implements SingleUserState<T> {
   private storageKey: string;
+  private updatePromise: Promise<T> | null = null;
+  private storageUpdateSubscription: Subscription;
+  private subscriberCount = new BehaviorSubject<number>(0);
+  private stateObservable: Observable<T>;
+  private reinitialize = false;
 
   protected stateSubject: BehaviorSubject<T | typeof FAKE_DEFAULT> = new BehaviorSubject<
     T | typeof FAKE_DEFAULT
   >(FAKE_DEFAULT);
 
-  state$: Observable<T>;
+  get state$() {
+    this.stateObservable = this.stateObservable ?? this.initializeObservable();
+    return this.stateObservable;
+  }
 
   constructor(
     readonly userId: UserId,
@@ -41,42 +48,6 @@ export class DefaultSingleUserState<T> implements SingleUserState<T> {
     private chosenLocation: AbstractStorageService & ObservableStorageService,
   ) {
     this.storageKey = userKeyBuilder(this.userId, this.keyDefinition);
-
-    const storageUpdates$ = this.chosenLocation.updates$.pipe(
-      filter((update) => update.key === this.storageKey),
-      switchMap(async (update) => {
-        if (update.updateType === "remove") {
-          return null;
-        }
-        return await getStoredValue(
-          this.storageKey,
-          this.chosenLocation,
-          this.keyDefinition.deserializer,
-        );
-      }),
-      shareReplay({ bufferSize: 1, refCount: false }),
-    );
-
-    this.state$ = defer(() => {
-      const storageUpdateSubscription = storageUpdates$.subscribe((value) => {
-        this.stateSubject.next(value);
-      });
-
-      this.getFromState().then((s) => {
-        this.stateSubject.next(s);
-      });
-
-      return this.stateSubject.pipe(
-        tap({
-          complete: () => {
-            storageUpdateSubscription.unsubscribe();
-          },
-        }),
-      );
-    }).pipe(
-      shareReplay({ refCount: false, bufferSize: 1 }),
-      filter<T>((i) => i != FAKE_DEFAULT),
-    );
   }
 
   async update<TCombine>(
@@ -84,7 +55,28 @@ export class DefaultSingleUserState<T> implements SingleUserState<T> {
     options: StateUpdateOptions<T, TCombine> = {},
   ): Promise<T> {
     options = populateOptionsWithDefault(options);
-    const currentState = await this.getGuaranteedState();
+    if (this.updatePromise != null) {
+      await this.updatePromise;
+    }
+
+    try {
+      this.updatePromise = this.internalUpdate(configureState, options);
+      const newState = await this.updatePromise;
+      return newState;
+    } finally {
+      this.updatePromise = null;
+    }
+  }
+
+  createDerived<TTo>(converter: Converter<T, TTo>): DerivedUserState<TTo> {
+    return new DefaultDerivedUserState<T, TTo>(converter, this.encryptService, this);
+  }
+
+  private async internalUpdate<TCombine>(
+    configureState: (state: T, dependency: TCombine) => T,
+    options: StateUpdateOptions<T, TCombine>,
+  ): Promise<T> {
+    const currentState = await this.getStateForUpdate();
     const combinedDependencies =
       options.combineLatestWith != null
         ? await firstValueFrom(options.combineLatestWith.pipe(timeout(options.msTimeout)))
@@ -99,20 +91,94 @@ export class DefaultSingleUserState<T> implements SingleUserState<T> {
     return newState;
   }
 
-  createDerived<TTo>(converter: Converter<T, TTo>): DerivedUserState<TTo> {
-    return new DefaultDerivedUserState<T, TTo>(converter, this.encryptService, this);
+  private initializeObservable() {
+    this.storageUpdateSubscription = this.chosenLocation.updates$
+      .pipe(
+        filter((update) => update.key === this.storageKey),
+        switchMap(async (update) => {
+          if (update.updateType === "remove") {
+            return null;
+          }
+          return await this.getFromState();
+        }),
+      )
+      .subscribe((v) => this.stateSubject.next(v));
+
+    this.subscriberCount.subscribe((count) => {
+      if (count === 0 && this.stateObservable != null) {
+        this.triggerCleanup();
+      }
+    });
+
+    // Intentionally un-awaited promise, we don't want to delay return of observable, but we do want to
+    // trigger populating it immediately.
+    this.getFromState().then((s) => {
+      this.stateSubject.next(s);
+    });
+
+    return new Observable<T>((subscriber) => {
+      this.incrementSubscribers();
+
+      // reinitialize listeners after cleanup
+      if (this.reinitialize) {
+        this.reinitialize = false;
+        this.initializeObservable();
+      }
+
+      const prevUnsubscribe = subscriber.unsubscribe.bind(subscriber);
+      subscriber.unsubscribe = () => {
+        this.decrementSubscribers();
+        prevUnsubscribe();
+      };
+
+      return this.stateSubject
+        .pipe(
+          // Filter out fake default, which is used to indicate that state is not ready to be emitted yet.
+          filter<T>((i) => i != FAKE_DEFAULT),
+        )
+        .subscribe(subscriber);
+    });
   }
 
-  private async getGuaranteedState() {
+  /** For use in update methods, does not wait for update to complete before yielding state.
+   * The expectation is that that await is already done
+   */
+  private async getStateForUpdate() {
     const currentValue = this.stateSubject.getValue();
-    return currentValue === FAKE_DEFAULT ? await this.getFromState() : currentValue;
+    return currentValue === FAKE_DEFAULT
+      ? await getStoredValue(this.storageKey, this.chosenLocation, this.keyDefinition.deserializer)
+      : currentValue;
   }
 
   async getFromState(): Promise<T> {
+    if (this.updatePromise != null) {
+      return await this.updatePromise;
+    }
     return await getStoredValue(
       this.storageKey,
       this.chosenLocation,
       this.keyDefinition.deserializer,
     );
   }
+
+  private incrementSubscribers() {
+    this.subscriberCount.next(this.subscriberCount.value + 1);
+  }
+
+  private decrementSubscribers() {
+    this.subscriberCount.next(this.subscriberCount.value - 1);
+  }
+
+  private triggerCleanup() {
+    setTimeout(() => {
+      if (this.subscriberCount.value === 0) {
+        this.updatePromise = null;
+        this.storageUpdateSubscription.unsubscribe();
+        this.subscriberCount.complete();
+        this.subscriberCount = new BehaviorSubject<number>(0);
+        this.stateSubject.next(FAKE_DEFAULT);
+        this.reinitialize = true;
+      }
+    }, this.keyDefinition.cleanupDelayMs);
+  }
 }
diff --git a/libs/common/src/platform/state/key-definition.spec.ts b/libs/common/src/platform/state/key-definition.spec.ts
index cbb1e49a9a1..ee926bccd8e 100644
--- a/libs/common/src/platform/state/key-definition.spec.ts
+++ b/libs/common/src/platform/state/key-definition.spec.ts
@@ -18,6 +18,37 @@ describe("KeyDefinition", () => {
     });
   });
 
+  describe("cleanupDelayMs", () => {
+    it("defaults to 1000ms", () => {
+      const keyDefinition = new KeyDefinition<boolean>(fakeStateDefinition, "fake", {
+        deserializer: (value) => value,
+      });
+
+      expect(keyDefinition).toBeTruthy();
+      expect(keyDefinition.cleanupDelayMs).toBe(1000);
+    });
+
+    it("can be overridden", () => {
+      const keyDefinition = new KeyDefinition<boolean>(fakeStateDefinition, "fake", {
+        deserializer: (value) => value,
+        cleanupDelayMs: 500,
+      });
+
+      expect(keyDefinition).toBeTruthy();
+      expect(keyDefinition.cleanupDelayMs).toBe(500);
+    });
+
+    it.each([0, -1])("throws on 0 or negative (%s)", (testValue: number) => {
+      expect(
+        () =>
+          new KeyDefinition<boolean>(fakeStateDefinition, "fake", {
+            deserializer: (value) => value,
+            cleanupDelayMs: testValue,
+          }),
+      ).toThrow();
+    });
+  });
+
   describe("record", () => {
     it("runs custom deserializer for each record value", () => {
       const recordDefinition = KeyDefinition.record<boolean>(fakeStateDefinition, "fake", {
diff --git a/libs/common/src/platform/state/key-definition.ts b/libs/common/src/platform/state/key-definition.ts
index db65740388e..9989bf37a24 100644
--- a/libs/common/src/platform/state/key-definition.ts
+++ b/libs/common/src/platform/state/key-definition.ts
@@ -19,6 +19,11 @@ type KeyDefinitionOptions<T> = {
    * @returns The fully typed version of your state.
    */
   readonly deserializer: (jsonValue: Jsonify<T>) => T;
+  /**
+   * The number of milliseconds to wait before cleaning up the state after the last subscriber has unsubscribed.
+   * Defaults to 1000ms.
+   */
+  readonly cleanupDelayMs?: number;
 };
 
 /**
@@ -42,8 +47,12 @@ export class KeyDefinition<T> {
     private readonly options: KeyDefinitionOptions<T>,
   ) {
     if (options.deserializer == null) {
+      throw new Error(`'deserializer' is a required property on key ${this.errorKeyName}`);
+    }
+
+    if (options.cleanupDelayMs <= 0) {
       throw new Error(
-        `'deserializer' is a required property on key ${stateDefinition.name} > ${key}`,
+        `'cleanupDelayMs' must be greater than 0. Value of ${options.cleanupDelayMs} passed to key ${this.errorKeyName} `,
       );
     }
   }
@@ -55,6 +64,13 @@ export class KeyDefinition<T> {
     return this.options.deserializer;
   }
 
+  /**
+   * Gets the number of milliseconds to wait before cleaning up the state after the last subscriber has unsubscribed.
+   */
+  get cleanupDelayMs() {
+    return this.options.cleanupDelayMs < 0 ? 0 : this.options.cleanupDelayMs ?? 1000;
+  }
+
   /**
    * Creates a {@link KeyDefinition} for state that is an array.
    * @param stateDefinition The state definition to be added to the KeyDefinition
@@ -137,6 +153,10 @@ export class KeyDefinition<T> {
       ? `${scope}_${userId}_${this.stateDefinition.name}_${this.key}`
       : `${scope}_${this.stateDefinition.name}_${this.key}`;
   }
+
+  private get errorKeyName() {
+    return `${this.stateDefinition.name} > ${this.key}`;
+  }
 }
 
 export type StorageKey = Opaque<string, "StorageKey">;
diff --git a/libs/importer/src/importers/passwordsafe-xml-importer.ts b/libs/importer/src/importers/passwordsafe-xml-importer.ts
index feefafec15d..8a6e3b629c7 100644
--- a/libs/importer/src/importers/passwordsafe-xml-importer.ts
+++ b/libs/importer/src/importers/passwordsafe-xml-importer.ts
@@ -3,6 +3,7 @@ import { ImportResult } from "../models/import-result";
 import { BaseImporter } from "./base-importer";
 import { Importer } from "./importer";
 
+/** This is the importer for the xml format from pwsafe.org  */
 export class PasswordSafeXmlImporter extends BaseImporter implements Importer {
   parse(data: string): Promise<ImportResult> {
     const result = new ImportResult();
diff --git a/libs/importer/src/models/import-options.ts b/libs/importer/src/models/import-options.ts
index fc0b4ce2bb7..64546cc57b3 100644
--- a/libs/importer/src/models/import-options.ts
+++ b/libs/importer/src/models/import-options.ts
@@ -29,7 +29,7 @@ export const regularImportOptions = [
   { id: "enpassjson", name: "Enpass (json)" },
   { id: "protonpass", name: "ProtonPass (zip/json)" },
   { id: "safeincloudxml", name: "SafeInCloud (xml)" },
-  { id: "pwsafexml", name: "Password Safe (xml)" },
+  { id: "pwsafexml", name: "Password Safe - pwsafe.org (xml)" },
   { id: "stickypasswordxml", name: "Sticky Password (xml)" },
   { id: "msecurecsv", name: "mSecure (csv)" },
   { id: "truekeycsv", name: "True Key (csv)" },
diff --git a/package-lock.json b/package-lock.json
index 1fdd961d5d0..ea8955f2adc 100644
--- a/package-lock.json
+++ b/package-lock.json
@@ -33,7 +33,7 @@
         "argon2-browser": "1.18.0",
         "big-integer": "1.6.51",
         "bootstrap": "4.6.0",
-        "braintree-web-drop-in": "1.40.0",
+        "braintree-web-drop-in": "1.41.0",
         "bufferutil": "4.0.8",
         "chalk": "4.1.2",
         "commander": "7.2.0",
@@ -4638,9 +4638,9 @@
       }
     },
     "node_modules/@braintree/browser-detection": {
-      "version": "1.14.0",
-      "resolved": "https://registry.npmjs.org/@braintree/browser-detection/-/browser-detection-1.14.0.tgz",
-      "integrity": "sha512-OsqU+28RhNvSw8Y5JEiUHUrAyn4OpYazFkjSJe8ZVZfkAaRXQc6hsV38MMEpIlkPMig+A68buk/diY+0O8/dMQ=="
+      "version": "1.17.1",
+      "resolved": "https://registry.npmjs.org/@braintree/browser-detection/-/browser-detection-1.17.1.tgz",
+      "integrity": "sha512-Mk7jauyp9pD14BTRS7otoy9dqIJGb3Oy0XtxKM/adGD9i9MAuCjH5uRZMyW2iVmJQTaA/PLlWdG7eSDyMWMc8Q=="
     },
     "node_modules/@braintree/event-emitter": {
       "version": "0.4.1",
@@ -4658,9 +4658,9 @@
       "integrity": "sha512-tVpr7U6u6bqeQlHreEjYMNtnHX62vLnNWziY2kQLqkWhvusPuY5DfuGEIPpWqsd+V/a1slyTQaxK6HWTlH6A/Q=="
     },
     "node_modules/@braintree/sanitize-url": {
-      "version": "6.0.2",
-      "resolved": "https://registry.npmjs.org/@braintree/sanitize-url/-/sanitize-url-6.0.2.tgz",
-      "integrity": "sha512-Tbsj02wXCbqGmzdnXNk0SOF19ChhRU70BsroIi4Pm6Ehp56in6vch94mfbdQ17DozxkL3BAVjbZ4Qc1a0HFRAg=="
+      "version": "6.0.4",
+      "resolved": "https://registry.npmjs.org/@braintree/sanitize-url/-/sanitize-url-6.0.4.tgz",
+      "integrity": "sha512-s3jaWicZd0pkP0jf5ysyHUI/RE7MHos6qlToFcGWXVp+ykHOy77OUMrfbgJ9it2C5bow7OIQwYYaHjk9XlBQ2A=="
     },
     "node_modules/@braintree/uuid": {
       "version": "0.1.0",
@@ -17244,16 +17244,16 @@
       }
     },
     "node_modules/braintree-web": {
-      "version": "3.96.1",
-      "resolved": "https://registry.npmjs.org/braintree-web/-/braintree-web-3.96.1.tgz",
-      "integrity": "sha512-e483TQkRmcO5zFH+pMGUokFWq5Q+Jyn9TmUIDofPpul1P+xOciwNqvekl/Ku6MsJBT1+kyH0cndBYMZVJpbrtg==",
+      "version": "3.97.4",
+      "resolved": "https://registry.npmjs.org/braintree-web/-/braintree-web-3.97.4.tgz",
+      "integrity": "sha512-w//M/ZI/MhjaxUwpICwZO50uTLF/L3WGLN4tFCPh/Xw20jDw8UBiM0Gzquq7gmwcQ1BgNnAAaYlR94HcSmt/Cg==",
       "dependencies": {
         "@braintree/asset-loader": "0.4.4",
-        "@braintree/browser-detection": "1.14.0",
+        "@braintree/browser-detection": "1.17.1",
         "@braintree/event-emitter": "0.4.1",
         "@braintree/extended-promise": "0.4.1",
         "@braintree/iframer": "1.1.0",
-        "@braintree/sanitize-url": "6.0.2",
+        "@braintree/sanitize-url": "6.0.4",
         "@braintree/uuid": "0.1.0",
         "@braintree/wrap-promise": "2.1.0",
         "card-validator": "8.1.1",
@@ -17265,16 +17265,16 @@
       }
     },
     "node_modules/braintree-web-drop-in": {
-      "version": "1.40.0",
-      "resolved": "https://registry.npmjs.org/braintree-web-drop-in/-/braintree-web-drop-in-1.40.0.tgz",
-      "integrity": "sha512-YrR+KitYu0X6+qkP2hvkjAolMJw3jKyd+Yppk+LZUFk1Bbfj7YayLjTQqLTyFT5MQmzpQKLYwbI75BBClPGc+Q==",
+      "version": "1.41.0",
+      "resolved": "https://registry.npmjs.org/braintree-web-drop-in/-/braintree-web-drop-in-1.41.0.tgz",
+      "integrity": "sha512-cpFY13iyoPNCTIOU7dipHmOvoblUtYFuA7ADAm0DUPk6oqxFz4EIr94R0Yg2rCabvjeauINDf01Y2d7/E1IaXg==",
       "dependencies": {
         "@braintree/asset-loader": "0.4.4",
-        "@braintree/browser-detection": "1.14.0",
+        "@braintree/browser-detection": "1.17.1",
         "@braintree/event-emitter": "0.4.1",
         "@braintree/uuid": "0.1.0",
         "@braintree/wrap-promise": "2.1.0",
-        "braintree-web": "3.96.1"
+        "braintree-web": "3.97.4"
       }
     },
     "node_modules/braintree-web/node_modules/promise-polyfill": {
diff --git a/package.json b/package.json
index 586612bcb9f..ecba301c142 100644
--- a/package.json
+++ b/package.json
@@ -165,7 +165,7 @@
     "argon2-browser": "1.18.0",
     "big-integer": "1.6.51",
     "bootstrap": "4.6.0",
-    "braintree-web-drop-in": "1.40.0",
+    "braintree-web-drop-in": "1.41.0",
     "bufferutil": "4.0.8",
     "chalk": "4.1.2",
     "commander": "7.2.0",