diff --git a/apps/browser/src/auth/popup/two-factor.component.ts b/apps/browser/src/auth/popup/two-factor.component.ts
index c0af31d25e5..a78f3d3de58 100644
--- a/apps/browser/src/auth/popup/two-factor.component.ts
+++ b/apps/browser/src/auth/popup/two-factor.component.ts
@@ -22,7 +22,9 @@ import { SyncService } from "@bitwarden/common/vault/abstractions/sync/sync.serv
 import { DialogService } from "@bitwarden/components";
 
 import { BrowserApi } from "../../platform/browser/browser-api";
-import { PopupUtilsService } from "../../popup/services/popup-utils.service";
+import BrowserPopupUtils from "../../platform/popup/browser-popup-utils";
+
+import { closeTwoFactorAuthPopout } from "./utils/auth-popout-window";
 
 const BroadcasterSubscriptionId = "TwoFactorComponent";
 
@@ -31,8 +33,6 @@ const BroadcasterSubscriptionId = "TwoFactorComponent";
   templateUrl: "two-factor.component.html",
 })
 export class TwoFactorComponent extends BaseTwoFactorComponent {
-  showNewWindowMessage = false;
-
   constructor(
     authService: AuthService,
     router: Router,
@@ -42,7 +42,6 @@ export class TwoFactorComponent extends BaseTwoFactorComponent {
     private syncService: SyncService,
     environmentService: EnvironmentService,
     private broadcasterService: BroadcasterService,
-    private popupUtilsService: PopupUtilsService,
     stateService: StateService,
     route: ActivatedRoute,
     private messagingService: MessagingService,
@@ -115,7 +114,7 @@ export class TwoFactorComponent extends BaseTwoFactorComponent {
 
     if (
       this.selectedProviderType === TwoFactorProviderType.Email &&
-      this.popupUtilsService.inPopup(window)
+      BrowserPopupUtils.inPopup(window)
     ) {
       const confirmed = await this.dialogService.openSimpleDialog({
         title: { key: "warning" },
@@ -123,7 +122,7 @@ export class TwoFactorComponent extends BaseTwoFactorComponent {
         type: "warning",
       });
       if (confirmed) {
-        this.popupUtilsService.popOut(window);
+        BrowserPopupUtils.openCurrentPagePopout(window);
       }
     }
 
@@ -142,7 +141,7 @@ export class TwoFactorComponent extends BaseTwoFactorComponent {
 
           // We don't need this window anymore because the intent is for the user to be left
           // on the web vault screen which tells them to continue in the browser extension (sidebar or popup)
-          BrowserApi.closeBitwardenExtensionTab();
+          await closeTwoFactorAuthPopout();
         };
       }
     });
diff --git a/apps/browser/src/auth/popup/utils/auth-popout-window.spec.ts b/apps/browser/src/auth/popup/utils/auth-popout-window.spec.ts
new file mode 100644
index 00000000000..1cc0d2948dc
--- /dev/null
+++ b/apps/browser/src/auth/popup/utils/auth-popout-window.spec.ts
@@ -0,0 +1,103 @@
+import { createChromeTabMock } from "../../../autofill/jest/autofill-mocks";
+import { BrowserApi } from "../../../platform/browser/browser-api";
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
+
+import {
+  AuthPopoutType,
+  openUnlockPopout,
+  closeUnlockPopout,
+  openSsoAuthResultPopout,
+  openTwoFactorAuthPopout,
+  closeTwoFactorAuthPopout,
+} from "./auth-popout-window";
+
+describe("AuthPopoutWindow", () => {
+  const openPopoutSpy = jest.spyOn(BrowserPopupUtils, "openPopout").mockImplementation();
+  const sendMessageDataSpy = jest.spyOn(BrowserApi, "tabSendMessageData").mockImplementation();
+  const closeSingleActionPopoutSpy = jest
+    .spyOn(BrowserPopupUtils, "closeSingleActionPopout")
+    .mockImplementation();
+
+  afterEach(() => {
+    jest.clearAllMocks();
+  });
+
+  describe("openUnlockPopout", () => {
+    it("opens a single action popup that allows the user to unlock the extension and sends a `bgUnlockPopoutOpened` message", async () => {
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValue([]);
+      const senderTab = { windowId: 1 } as chrome.tabs.Tab;
+
+      await openUnlockPopout(senderTab);
+
+      expect(openPopoutSpy).toHaveBeenCalledWith("popup/index.html", {
+        singleActionKey: AuthPopoutType.unlockExtension,
+        senderWindowId: 1,
+      });
+      expect(sendMessageDataSpy).toHaveBeenCalledWith(senderTab, "bgUnlockPopoutOpened");
+    });
+
+    it("closes any existing popup window types that are open to the unlock extension route", async () => {
+      const unlockTab = createChromeTabMock({
+        url: chrome.runtime.getURL("popup/index.html#/lock"),
+      });
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValue([unlockTab]);
+      jest.spyOn(BrowserApi, "removeWindow");
+      const senderTab = { windowId: 1 } as chrome.tabs.Tab;
+
+      await openUnlockPopout(senderTab);
+
+      expect(BrowserApi.tabsQuery).toHaveBeenCalledWith({ windowType: "popup" });
+      expect(BrowserApi.removeWindow).toHaveBeenCalledWith(unlockTab.windowId);
+    });
+
+    it("closes any existing popup window types that are open to the login extension route", async () => {
+      const loginTab = createChromeTabMock({
+        url: chrome.runtime.getURL("popup/index.html#/home"),
+      });
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValue([loginTab]);
+      jest.spyOn(BrowserApi, "removeWindow");
+      const senderTab = { windowId: 1 } as chrome.tabs.Tab;
+
+      await openUnlockPopout(senderTab);
+
+      expect(BrowserApi.removeWindow).toHaveBeenCalledWith(loginTab.windowId);
+    });
+  });
+
+  describe("closeUnlockPopout", () => {
+    it("closes the unlock extension popout window", () => {
+      closeUnlockPopout();
+
+      expect(closeSingleActionPopoutSpy).toHaveBeenCalledWith("auth_unlockExtension");
+    });
+  });
+
+  describe("openSsoAuthResultPopout", () => {
+    it("opens a window that facilitates presentation of the results for SSO authentication", () => {
+      openSsoAuthResultPopout({ code: "code", state: "state" });
+
+      expect(openPopoutSpy).toHaveBeenCalledWith("popup/index.html#/sso?code=code&state=state", {
+        singleActionKey: AuthPopoutType.ssoAuthResult,
+      });
+    });
+  });
+
+  describe("openTwoFactorAuthPopout", () => {
+    it("opens a window that facilitates two factor authentication", () => {
+      openTwoFactorAuthPopout({ data: "data", remember: "remember" });
+
+      expect(openPopoutSpy).toHaveBeenCalledWith(
+        "popup/index.html#/2fa;webAuthnResponse=data;remember=remember",
+        { singleActionKey: AuthPopoutType.twoFactorAuth }
+      );
+    });
+  });
+
+  describe("closeTwoFactorAuthPopout", () => {
+    it("closes the two-factor authentication window", () => {
+      closeTwoFactorAuthPopout();
+
+      expect(closeSingleActionPopoutSpy).toHaveBeenCalledWith("auth_twoFactorAuth");
+    });
+  });
+});
diff --git a/apps/browser/src/auth/popup/utils/auth-popout-window.ts b/apps/browser/src/auth/popup/utils/auth-popout-window.ts
new file mode 100644
index 00000000000..2f995fc1f4a
--- /dev/null
+++ b/apps/browser/src/auth/popup/utils/auth-popout-window.ts
@@ -0,0 +1,87 @@
+import { BrowserApi } from "../../../platform/browser/browser-api";
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
+
+const AuthPopoutType = {
+  unlockExtension: "auth_unlockExtension",
+  ssoAuthResult: "auth_ssoAuthResult",
+  twoFactorAuth: "auth_twoFactorAuth",
+} as const;
+const extensionUnlockUrls = new Set([
+  chrome.runtime.getURL("popup/index.html#/lock"),
+  chrome.runtime.getURL("popup/index.html#/home"),
+]);
+
+/**
+ * Opens a window that facilitates unlocking / logging into the extension.
+ *
+ * @param senderTab - Used to determine the windowId of the sender.
+ */
+async function openUnlockPopout(senderTab: chrome.tabs.Tab) {
+  const existingPopoutWindowTabs = await BrowserApi.tabsQuery({ windowType: "popup" });
+  existingPopoutWindowTabs.forEach((tab) => {
+    if (extensionUnlockUrls.has(tab.url)) {
+      BrowserApi.removeWindow(tab.windowId);
+    }
+  });
+
+  await BrowserPopupUtils.openPopout("popup/index.html", {
+    singleActionKey: AuthPopoutType.unlockExtension,
+    senderWindowId: senderTab.windowId,
+  });
+  await BrowserApi.tabSendMessageData(senderTab, "bgUnlockPopoutOpened");
+}
+
+/**
+ * Closes the unlock popout window.
+ */
+async function closeUnlockPopout() {
+  await BrowserPopupUtils.closeSingleActionPopout(AuthPopoutType.unlockExtension);
+}
+
+/**
+ * Opens a window that facilitates presenting the results for SSO authentication.
+ *
+ * @param resultData - The result data from the SSO authentication.
+ */
+async function openSsoAuthResultPopout(resultData: { code: string; state: string }) {
+  const { code, state } = resultData;
+  const authResultUrl = `popup/index.html#/sso?code=${encodeURIComponent(
+    code
+  )}&state=${encodeURIComponent(state)}`;
+
+  await BrowserPopupUtils.openPopout(authResultUrl, {
+    singleActionKey: AuthPopoutType.ssoAuthResult,
+  });
+}
+
+/**
+ * Opens a window that facilitates two-factor authentication.
+ *
+ * @param twoFactorAuthData - The data from the two-factor authentication.
+ */
+async function openTwoFactorAuthPopout(twoFactorAuthData: { data: string; remember: string }) {
+  const { data, remember } = twoFactorAuthData;
+  const params =
+    `webAuthnResponse=${encodeURIComponent(data)};` + `remember=${encodeURIComponent(remember)}`;
+  const twoFactorUrl = `popup/index.html#/2fa;${params}`;
+
+  await BrowserPopupUtils.openPopout(twoFactorUrl, {
+    singleActionKey: AuthPopoutType.twoFactorAuth,
+  });
+}
+
+/**
+ * Closes the two-factor authentication popout window.
+ */
+async function closeTwoFactorAuthPopout() {
+  await BrowserPopupUtils.closeSingleActionPopout(AuthPopoutType.twoFactorAuth);
+}
+
+export {
+  AuthPopoutType,
+  openUnlockPopout,
+  closeUnlockPopout,
+  openSsoAuthResultPopout,
+  openTwoFactorAuthPopout,
+  closeTwoFactorAuthPopout,
+};
diff --git a/apps/browser/src/autofill/background/notification.background.ts b/apps/browser/src/autofill/background/notification.background.ts
index f95ca60bab1..dada3430af5 100644
--- a/apps/browser/src/autofill/background/notification.background.ts
+++ b/apps/browser/src/autofill/background/notification.background.ts
@@ -12,6 +12,7 @@ import { FolderService } from "@bitwarden/common/vault/abstractions/folder/folde
 import { CipherType } from "@bitwarden/common/vault/enums/cipher-type";
 import { CipherView } from "@bitwarden/common/vault/models/view/cipher.view";
 
+import { openUnlockPopout } from "../../auth/popup/utils/auth-popout-window";
 import AddUnlockVaultQueueMessage from "../../background/models/add-unlock-vault-queue-message";
 import AddChangePasswordQueueMessage from "../../background/models/addChangePasswordQueueMessage";
 import AddLoginQueueMessage from "../../background/models/addLoginQueueMessage";
@@ -21,6 +22,7 @@ import LockedVaultPendingNotificationsItem from "../../background/models/lockedV
 import { NotificationQueueMessageType } from "../../background/models/notificationQueueMessageType";
 import { BrowserApi } from "../../platform/browser/browser-api";
 import { BrowserStateService } from "../../platform/services/abstractions/browser-state.service";
+import { openAddEditVaultItemPopout } from "../../vault/popup/utils/vault-popout-window";
 import { AutofillService } from "../services/abstractions/autofill.service";
 
 export default class NotificationBackground {
@@ -96,7 +98,7 @@ export default class NotificationBackground {
             "addToLockedVaultPendingNotifications",
             retryMessage
           );
-          await BrowserApi.tabSendMessageData(sender.tab, "promptForLogin");
+          await openUnlockPopout(sender.tab);
           return;
         }
         await this.saveOrUpdateCredentials(sender.tab, msg.edit, msg.folder);
@@ -118,9 +120,12 @@ export default class NotificationBackground {
             break;
         }
         break;
-      case "promptForLogin":
+      case "bgUnlockPopoutOpened":
         await this.unlockVault(sender.tab);
         break;
+      case "bgReopenUnlockPopout":
+        await openUnlockPopout(sender.tab);
+        break;
       default:
         break;
     }
@@ -447,9 +452,7 @@ export default class NotificationBackground {
       collectionIds: cipherView.collectionIds,
     });
 
-    await BrowserApi.tabSendMessageData(senderTab, "openAddEditCipher", {
-      cipherId: cipherView.id,
-    });
+    await openAddEditVaultItemPopout(senderTab, { cipherId: cipherView.id });
   }
 
   private async folderExists(folderId: string) {
diff --git a/apps/browser/src/autofill/browser/context-menu-clicked-handler.ts b/apps/browser/src/autofill/browser/context-menu-clicked-handler.ts
index 54c3e244991..e7f57a46869 100644
--- a/apps/browser/src/autofill/browser/context-menu-clicked-handler.ts
+++ b/apps/browser/src/autofill/browser/context-menu-clicked-handler.ts
@@ -18,6 +18,7 @@ import {
 } from "../../auth/background/service-factories/auth-service.factory";
 import { totpServiceFactory } from "../../auth/background/service-factories/totp-service.factory";
 import { userVerificationServiceFactory } from "../../auth/background/service-factories/user-verification-service.factory";
+import { openUnlockPopout } from "../../auth/popup/utils/auth-popout-window";
 import LockedVaultPendingNotificationsItem from "../../background/models/lockedVaultPendingNotificationsItem";
 import { eventCollectionServiceFactory } from "../../background/service-factories/event-collection-service.factory";
 import { Account } from "../../models/account";
@@ -29,6 +30,10 @@ import {
   cipherServiceFactory,
   CipherServiceInitOptions,
 } from "../../vault/background/service_factories/cipher-service.factory";
+import {
+  openAddEditVaultItemPopout,
+  openVaultItemPasswordRepromptPopout,
+} from "../../vault/popup/utils/vault-popout-window";
 import { autofillServiceFactory } from "../background/service_factories/autofill-service.factory";
 import { copyToClipboard, GeneratePasswordToClipboardCommand } from "../clipboard";
 import { AutofillTabCommand } from "../commands/autofill-tab-command";
@@ -187,7 +192,7 @@ export class ContextMenuClickedHandler {
         retryMessage
       );
 
-      await BrowserApi.tabSendMessageData(tab, "promptForLogin");
+      await openUnlockPopout(tab);
       return;
     }
 
@@ -235,14 +240,12 @@ export class ContextMenuClickedHandler {
         const cipherType = this.getCipherCreationType(menuItemId);
 
         if (cipherType) {
-          await BrowserApi.tabSendMessageData(tab, "openAddEditCipher", {
-            cipherType,
-          });
+          await openAddEditVaultItemPopout(tab, { cipherType });
           break;
         }
 
         if (await this.isPasswordRepromptRequired(cipher)) {
-          await BrowserApi.tabSendMessageData(tab, "passwordReprompt", {
+          await openVaultItemPasswordRepromptPopout(tab, {
             cipherId: cipher.id,
             // The action here is passed on to the single-use reprompt window and doesn't change based on cipher type
             action: AUTOFILL_ID,
@@ -255,9 +258,7 @@ export class ContextMenuClickedHandler {
       }
       case COPY_USERNAME_ID:
         if (menuItemId === CREATE_LOGIN_ID) {
-          await BrowserApi.tabSendMessageData(tab, "openAddEditCipher", {
-            cipherType: CipherType.Login,
-          });
+          await openAddEditVaultItemPopout(tab, { cipherType: CipherType.Login });
           break;
         }
 
@@ -265,16 +266,14 @@ export class ContextMenuClickedHandler {
         break;
       case COPY_PASSWORD_ID:
         if (menuItemId === CREATE_LOGIN_ID) {
-          await BrowserApi.tabSendMessageData(tab, "openAddEditCipher", {
-            cipherType: CipherType.Login,
-          });
+          await openAddEditVaultItemPopout(tab, { cipherType: CipherType.Login });
           break;
         }
 
         if (await this.isPasswordRepromptRequired(cipher)) {
-          await BrowserApi.tabSendMessageData(tab, "passwordReprompt", {
+          await openVaultItemPasswordRepromptPopout(tab, {
             cipherId: cipher.id,
-            action: info.parentMenuItemId,
+            action: COPY_PASSWORD_ID,
           });
         } else {
           this.copyToClipboard({ text: cipher.login.password, tab: tab });
@@ -284,16 +283,14 @@ export class ContextMenuClickedHandler {
         break;
       case COPY_VERIFICATIONCODE_ID:
         if (menuItemId === CREATE_LOGIN_ID) {
-          await BrowserApi.tabSendMessageData(tab, "openAddEditCipher", {
-            cipherType: CipherType.Login,
-          });
+          await openAddEditVaultItemPopout(tab, { cipherType: CipherType.Login });
           break;
         }
 
         if (await this.isPasswordRepromptRequired(cipher)) {
-          await BrowserApi.tabSendMessageData(tab, "passwordReprompt", {
+          await openVaultItemPasswordRepromptPopout(tab, {
             cipherId: cipher.id,
-            action: info.parentMenuItemId,
+            action: COPY_VERIFICATIONCODE_ID,
           });
         } else {
           this.copyToClipboard({
diff --git a/apps/browser/src/autofill/content/message_handler.ts b/apps/browser/src/autofill/content/message_handler.ts
index 3fdf0f20124..c2c5c4d3196 100644
--- a/apps/browser/src/autofill/content/message_handler.ts
+++ b/apps/browser/src/autofill/content/message_handler.ts
@@ -28,12 +28,10 @@ window.addEventListener(
 );
 
 const forwardCommands = [
-  "promptForLogin",
-  "passwordReprompt",
+  "bgUnlockPopoutOpened",
   "addToLockedVaultPendingNotifications",
   "unlockCompleted",
   "addedCipher",
-  "openAddEditCipher",
 ];
 
 chrome.runtime.onMessage.addListener((event) => {
diff --git a/apps/browser/src/autofill/notification/bar.ts b/apps/browser/src/autofill/notification/bar.ts
index dcc4ce010f6..f4110d6dad2 100644
--- a/apps/browser/src/autofill/notification/bar.ts
+++ b/apps/browser/src/autofill/notification/bar.ts
@@ -189,7 +189,7 @@ function handleTypeUnlock() {
   const unlockButton = document.getElementById("unlock-vault");
   unlockButton.addEventListener("click", (e) => {
     sendPlatformMessage({
-      command: "bgReopenPromptForLogin",
+      command: "bgReopenUnlockPopout",
     });
   });
 }
diff --git a/apps/browser/src/autofill/services/autofill.service.spec.ts b/apps/browser/src/autofill/services/autofill.service.spec.ts
index 544b0da1a5c..446aae6420d 100644
--- a/apps/browser/src/autofill/services/autofill.service.spec.ts
+++ b/apps/browser/src/autofill/services/autofill.service.spec.ts
@@ -752,13 +752,15 @@ describe("AutofillService", () => {
         jest
           .spyOn(userVerificationService, "hasMasterPasswordAndMasterKeyHash")
           .mockResolvedValueOnce(true);
-        jest.spyOn(BrowserApi, "tabSendMessageData").mockImplementation();
+        jest
+          .spyOn(autofillService as any, "openVaultItemPasswordRepromptPopout")
+          .mockImplementation();
 
         const result = await autofillService.doAutoFillOnTab(pageDetails, tab, true);
 
         expect(cipherService.getNextCipherForUrl).toHaveBeenCalledWith(tab.url);
         expect(userVerificationService.hasMasterPasswordAndMasterKeyHash).toHaveBeenCalled();
-        expect(BrowserApi.tabSendMessageData).toHaveBeenCalledWith(tab, "passwordReprompt", {
+        expect(autofillService["openVaultItemPasswordRepromptPopout"]).toHaveBeenCalledWith(tab, {
           cipherId: cipher.id,
           action: "autofill",
         });
@@ -4254,4 +4256,24 @@ describe("AutofillService", () => {
       expect(result).toBe(false);
     });
   });
+
+  describe("isDebouncingPasswordRepromptPopout", () => {
+    it("returns false and sets up the debounce if a master password reprompt window is not currently opening", () => {
+      jest.spyOn(globalThis, "setTimeout");
+
+      const result = autofillService["isDebouncingPasswordRepromptPopout"]();
+
+      expect(result).toBe(false);
+      expect(globalThis.setTimeout).toHaveBeenCalledWith(expect.any(Function), 100);
+      expect(autofillService["currentlyOpeningPasswordRepromptPopout"]).toBe(true);
+    });
+
+    it("returns true if a master password reprompt window is currently opening", () => {
+      autofillService["currentlyOpeningPasswordRepromptPopout"] = true;
+
+      const result = autofillService["isDebouncingPasswordRepromptPopout"]();
+
+      expect(result).toBe(true);
+    });
+  });
 });
diff --git a/apps/browser/src/autofill/services/autofill.service.ts b/apps/browser/src/autofill/services/autofill.service.ts
index 8ab20027756..a506425bc39 100644
--- a/apps/browser/src/autofill/services/autofill.service.ts
+++ b/apps/browser/src/autofill/services/autofill.service.ts
@@ -12,6 +12,7 @@ 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 AutofillField from "../models/autofill-field";
 import AutofillPageDetails from "../models/autofill-page-details";
 import AutofillScript from "../models/autofill-script";
@@ -30,6 +31,10 @@ import {
 } from "./autofill-constants";
 
 export default class AutofillService implements AutofillServiceInterface {
+  private openVaultItemPasswordRepromptPopout = openVaultItemPasswordRepromptPopout;
+  private openPasswordRepromptPopoutDebounce: NodeJS.Timeout;
+  private currentlyOpeningPasswordRepromptPopout = false;
+
   constructor(
     private cipherService: CipherService,
     private stateService: BrowserStateService,
@@ -272,13 +277,14 @@ export default class AutofillService implements AutofillServiceInterface {
     if (
       cipher.reprompt === CipherRepromptType.Password &&
       // If the master password has is not available, reprompt will error
-      (await this.userVerificationService.hasMasterPasswordAndMasterKeyHash())
+      (await this.userVerificationService.hasMasterPasswordAndMasterKeyHash()) &&
+      !this.isDebouncingPasswordRepromptPopout()
     ) {
       if (fromCommand) {
         this.cipherService.updateLastUsedIndexForUrl(tab.url);
       }
 
-      await BrowserApi.tabSendMessageData(tab, "passwordReprompt", {
+      await this.openVaultItemPasswordRepromptPopout(tab, {
         cipherId: cipher.id,
         action: "autofill",
       });
@@ -1828,4 +1834,22 @@ export default class AutofillService implements AutofillServiceInterface {
   static forCustomFieldsOnly(field: AutofillField): boolean {
     return field.tagName === "span";
   }
+
+  /**
+   * Handles debouncing the opening of the master password reprompt popout.
+   */
+  private isDebouncingPasswordRepromptPopout() {
+    if (this.currentlyOpeningPasswordRepromptPopout) {
+      return true;
+    }
+
+    this.currentlyOpeningPasswordRepromptPopout = true;
+    clearTimeout(this.openPasswordRepromptPopoutDebounce);
+
+    this.openPasswordRepromptPopoutDebounce = setTimeout(() => {
+      this.currentlyOpeningPasswordRepromptPopout = false;
+    }, 100);
+
+    return false;
+  }
 }
diff --git a/apps/browser/src/background/commands.background.ts b/apps/browser/src/background/commands.background.ts
index 77300272d26..210119aa5f2 100644
--- a/apps/browser/src/background/commands.background.ts
+++ b/apps/browser/src/background/commands.background.ts
@@ -4,6 +4,7 @@ import { AuthenticationStatus } from "@bitwarden/common/auth/enums/authenticatio
 import { PlatformUtilsService } from "@bitwarden/common/platform/abstractions/platform-utils.service";
 import { PasswordGenerationServiceAbstraction } from "@bitwarden/common/tools/generator/password";
 
+import { openUnlockPopout } from "../auth/popup/utils/auth-popout-window";
 import { BrowserApi } from "../platform/browser/browser-api";
 
 import MainBackground from "./main.background";
@@ -87,7 +88,7 @@ export default class CommandsBackground {
         retryMessage
       );
 
-      BrowserApi.tabSendMessageData(tab, "promptForLogin");
+      await openUnlockPopout(tab);
       return;
     }
 
diff --git a/apps/browser/src/background/main.background.ts b/apps/browser/src/background/main.background.ts
index e82a09ba008..e3fe610fce5 100644
--- a/apps/browser/src/background/main.background.ts
+++ b/apps/browser/src/background/main.background.ts
@@ -132,7 +132,6 @@ import { Account } from "../models/account";
 import { BrowserApi } from "../platform/browser/browser-api";
 import { flagEnabled } from "../platform/flags";
 import { UpdateBadge } from "../platform/listeners/update-badge";
-import BrowserPopoutWindowService from "../platform/popup/browser-popout-window.service";
 import { BrowserStateService as StateServiceAbstraction } from "../platform/services/abstractions/browser-state.service";
 import { BrowserConfigService } from "../platform/services/browser-config.service";
 import { BrowserCryptoService } from "../platform/services/browser-crypto.service";
@@ -145,7 +144,6 @@ import BrowserPlatformUtilsService from "../platform/services/browser-platform-u
 import { BrowserStateService } from "../platform/services/browser-state.service";
 import { KeyGenerationService } from "../platform/services/key-generation.service";
 import { LocalBackedSessionStorageService } from "../platform/services/local-backed-session-storage.service";
-import { PopupUtilsService } from "../popup/services/popup-utils.service";
 import { BrowserSendService } from "../services/browser-send.service";
 import { BrowserSettingsService } from "../services/browser-settings.service";
 import VaultTimeoutService from "../services/vault-timeout/vault-timeout.service";
@@ -225,8 +223,6 @@ export default class MainBackground {
   devicesService: DevicesServiceAbstraction;
   deviceTrustCryptoService: DeviceTrustCryptoServiceAbstraction;
   authRequestCryptoService: AuthRequestCryptoServiceAbstraction;
-  popupUtilsService: PopupUtilsService;
-  browserPopoutWindowService: BrowserPopoutWindowService;
   accountService: AccountServiceAbstraction;
 
   // Passed to the popup for Safari to workaround issues with theming, downloading, etc.
@@ -583,12 +579,7 @@ export default class MainBackground {
       this.messagingService
     );
 
-    this.browserPopoutWindowService = new BrowserPopoutWindowService();
-
-    this.fido2UserInterfaceService = new BrowserFido2UserInterfaceService(
-      this.browserPopoutWindowService,
-      this.authService
-    );
+    this.fido2UserInterfaceService = new BrowserFido2UserInterfaceService(this.authService);
     this.fido2AuthenticatorService = new Fido2AuthenticatorService(
       this.cipherService,
       this.fido2UserInterfaceService,
@@ -634,8 +625,7 @@ export default class MainBackground {
       this.environmentService,
       this.messagingService,
       this.logService,
-      this.configService,
-      this.browserPopoutWindowService
+      this.configService
     );
     this.nativeMessagingBackground = new NativeMessagingBackground(
       this.cryptoService,
diff --git a/apps/browser/src/background/runtime.background.ts b/apps/browser/src/background/runtime.background.ts
index 83764da49d5..9d8ab4b898d 100644
--- a/apps/browser/src/background/runtime.background.ts
+++ b/apps/browser/src/background/runtime.background.ts
@@ -8,9 +8,13 @@ import { SystemService } from "@bitwarden/common/platform/abstractions/system.se
 import { Utils } from "@bitwarden/common/platform/misc/utils";
 import { CipherType } from "@bitwarden/common/vault/enums/cipher-type";
 
+import {
+  closeUnlockPopout,
+  openSsoAuthResultPopout,
+  openTwoFactorAuthPopout,
+} from "../auth/popup/utils/auth-popout-window";
 import { AutofillService } from "../autofill/services/abstractions/autofill.service";
 import { BrowserApi } from "../platform/browser/browser-api";
-import { BrowserPopoutWindowService } from "../platform/popup/abstractions/browser-popout-window.service";
 import { BrowserStateService } from "../platform/services/abstractions/browser-state.service";
 import { BrowserEnvironmentService } from "../platform/services/browser-environment.service";
 import BrowserPlatformUtilsService from "../platform/services/browser-platform-utils.service";
@@ -37,8 +41,7 @@ export default class RuntimeBackground {
     private environmentService: BrowserEnvironmentService,
     private messagingService: MessagingService,
     private logService: LogService,
-    private configService: ConfigServiceAbstraction,
-    private browserPopoutWindowService: BrowserPopoutWindowService
+    private configService: ConfigServiceAbstraction
   ) {
     // onInstalled listener must be wired up before anything else, so we do it in the ctor
     chrome.runtime.onInstalled.addListener((details: any) => {
@@ -82,8 +85,6 @@ export default class RuntimeBackground {
   }
 
   async processMessage(msg: any, sender: chrome.runtime.MessageSender) {
-    const cipherId = msg.data?.cipherId;
-
     switch (msg.command) {
       case "loggedIn":
       case "unlocked": {
@@ -91,7 +92,7 @@ export default class RuntimeBackground {
 
         if (this.lockedVaultPendingNotifications?.length > 0) {
           item = this.lockedVaultPendingNotifications.pop();
-          await this.browserPopoutWindowService.closeUnlockPrompt();
+          await closeUnlockPopout();
         }
 
         await this.main.refreshBadge();
@@ -129,49 +130,6 @@ export default class RuntimeBackground {
       case "openPopup":
         await this.main.openPopup();
         break;
-      case "promptForLogin":
-      case "bgReopenPromptForLogin":
-        await this.browserPopoutWindowService.openUnlockPrompt(sender.tab?.windowId);
-        break;
-      case "passwordReprompt":
-        if (cipherId) {
-          await this.browserPopoutWindowService.openPasswordRepromptPrompt(sender.tab?.windowId, {
-            cipherId: cipherId,
-            senderTabId: sender.tab.id,
-            action: msg.data?.action,
-          });
-        }
-        break;
-      case "openAddEditCipher": {
-        const isNewCipher = !cipherId;
-        const cipherType = msg.data?.cipherType;
-        const senderTab = sender.tab;
-
-        if (!senderTab) {
-          break;
-        }
-
-        if (isNewCipher) {
-          await this.browserPopoutWindowService.openCipherCreation(senderTab.windowId, {
-            cipherType,
-            senderTabId: senderTab.id,
-            senderTabURI: senderTab.url,
-          });
-        } else {
-          await this.browserPopoutWindowService.openCipherEdit(senderTab.windowId, {
-            cipherId,
-            senderTabId: senderTab.id,
-            senderTabURI: senderTab.url,
-          });
-        }
-
-        break;
-      }
-      case "closeTab":
-        setTimeout(() => {
-          BrowserApi.closeBitwardenExtensionTab();
-        }, msg.delay ?? 0);
-        break;
       case "triggerAutofillScriptInjection":
         await this.autofillService.injectAutofillScripts(
           sender,
@@ -266,12 +224,7 @@ export default class RuntimeBackground {
           });
         } else {
           try {
-            BrowserApi.createNewTab(
-              "popup/index.html?uilocation=popout#/sso?code=" +
-                encodeURIComponent(msg.code) +
-                "&state=" +
-                encodeURIComponent(msg.state)
-            );
+            await openSsoAuthResultPopout(msg);
           } catch {
             this.logService.error("Unable to open sso popout tab");
           }
@@ -285,10 +238,7 @@ export default class RuntimeBackground {
           return;
         }
 
-        const params =
-          `webAuthnResponse=${encodeURIComponent(msg.data)};` +
-          `remember=${encodeURIComponent(msg.remember)}`;
-        BrowserApi.openBitwardenExtensionTab(`popup/index.html#/2fa;${params}`, false);
+        await openTwoFactorAuthPopout(msg);
         break;
       }
       case "reloadPopup":
diff --git a/apps/browser/src/platform/browser/browser-api.spec.ts b/apps/browser/src/platform/browser/browser-api.spec.ts
index af9e633a7f1..057ae0a1010 100644
--- a/apps/browser/src/platform/browser/browser-api.spec.ts
+++ b/apps/browser/src/platform/browser/browser-api.spec.ts
@@ -9,6 +9,89 @@ describe("BrowserApi", () => {
     jest.clearAllMocks();
   });
 
+  describe("getWindow", () => {
+    it("will get the current window if a window id is not provided", () => {
+      BrowserApi.getWindow();
+
+      expect(chrome.windows.getCurrent).toHaveBeenCalledWith({ populate: true }, expect.anything());
+    });
+
+    it("will get the window with the provided id if one is provided", () => {
+      const windowId = 1;
+
+      BrowserApi.getWindow(windowId);
+
+      expect(chrome.windows.get).toHaveBeenCalledWith(
+        windowId,
+        { populate: true },
+        expect.anything()
+      );
+    });
+  });
+
+  describe("getCurrentWindow", () => {
+    it("will get the current window", () => {
+      BrowserApi.getCurrentWindow();
+
+      expect(chrome.windows.getCurrent).toHaveBeenCalledWith({ populate: true }, expect.anything());
+    });
+  });
+
+  describe("getWindowById", () => {
+    it("will get the window associated with the passed window id", () => {
+      const windowId = 1;
+
+      BrowserApi.getWindowById(windowId);
+
+      expect(chrome.windows.get).toHaveBeenCalledWith(
+        windowId,
+        { populate: true },
+        expect.anything()
+      );
+    });
+  });
+
+  describe("removeWindow", () => {
+    it("removes the window based on the passed window id", () => {
+      const windowId = 10;
+
+      BrowserApi.removeWindow(windowId);
+
+      expect(chrome.windows.remove).toHaveBeenCalledWith(windowId, expect.anything());
+    });
+  });
+
+  describe("updateWindowProperties", () => {
+    it("will update the window with the provided window options", () => {
+      const windowId = 1;
+      const windowOptions: chrome.windows.UpdateInfo = {
+        focused: true,
+      };
+
+      BrowserApi.updateWindowProperties(windowId, windowOptions);
+
+      expect(chrome.windows.update).toHaveBeenCalledWith(
+        windowId,
+        windowOptions,
+        expect.anything()
+      );
+    });
+  });
+
+  describe("focusWindow", () => {
+    it("will focus the window with the provided window id", () => {
+      const windowId = 1;
+
+      BrowserApi.focusWindow(windowId);
+
+      expect(chrome.windows.update).toHaveBeenCalledWith(
+        windowId,
+        { focused: true },
+        expect.anything()
+      );
+    });
+  });
+
   describe("executeScriptInTab", () => {
     it("calls to the extension api to execute a script within the give tabId", async () => {
       const tabId = 1;
diff --git a/apps/browser/src/platform/browser/browser-api.ts b/apps/browser/src/platform/browser/browser-api.ts
index dce72f5cf65..64efbfdc571 100644
--- a/apps/browser/src/platform/browser/browser-api.ts
+++ b/apps/browser/src/platform/browser/browser-api.ts
@@ -19,14 +19,33 @@ export class BrowserApi {
     return chrome.runtime.getManifest().manifest_version;
   }
 
-  static getWindow(windowId?: number): Promise<chrome.windows.Window> | void {
+  /**
+   * Gets the current window or the window with the given id.
+   *
+   * @param windowId - The id of the window to get. If not provided, the current window is returned.
+   */
+  static async getWindow(windowId?: number): Promise<chrome.windows.Window> {
     if (!windowId) {
-      return;
+      return BrowserApi.getCurrentWindow();
     }
 
-    return new Promise((resolve) =>
-      chrome.windows.get(windowId, { populate: true }, (window) => resolve(window))
-    );
+    return await BrowserApi.getWindowById(windowId);
+  }
+
+  /**
+   * Gets the currently active browser window.
+   */
+  static async getCurrentWindow(): Promise<chrome.windows.Window> {
+    return new Promise((resolve) => chrome.windows.getCurrent({ populate: true }, resolve));
+  }
+
+  /**
+   * Gets the window with the given id.
+   *
+   * @param windowId - The id of the window to get.
+   */
+  static async getWindowById(windowId: number): Promise<chrome.windows.Window> {
+    return new Promise((resolve) => chrome.windows.get(windowId, { populate: true }, resolve));
   }
 
   static async createWindow(options: chrome.windows.CreateData): Promise<chrome.windows.Window> {
@@ -37,8 +56,39 @@ export class BrowserApi {
     );
   }
 
-  static async removeWindow(windowId: number) {
-    await chrome.windows.remove(windowId);
+  /**
+   * Removes the window with the given id.
+   *
+   * @param windowId - The id of the window to remove.
+   */
+  static async removeWindow(windowId: number): Promise<void> {
+    return new Promise((resolve) => chrome.windows.remove(windowId, () => resolve()));
+  }
+
+  /**
+   * Updates the properties of the window with the given id.
+   *
+   * @param windowId - The id of the window to update.
+   * @param options - The window properties to update.
+   */
+  static async updateWindowProperties(
+    windowId: number,
+    options: chrome.windows.UpdateInfo
+  ): Promise<void> {
+    return new Promise((resolve) =>
+      chrome.windows.update(windowId, options, () => {
+        resolve();
+      })
+    );
+  }
+
+  /**
+   * Focuses the window with the given id.
+   *
+   * @param windowId - The id of the window to focus.
+   */
+  static async focusWindow(windowId: number) {
+    await BrowserApi.updateWindowProperties(windowId, { focused: true });
   }
 
   static async getTabFromCurrentWindowId(): Promise<chrome.tabs.Tab> | null {
@@ -138,10 +188,6 @@ export class BrowserApi {
     chrome.tabs.sendMessage<TabMessage, T>(tabId, message, options, responseCallback);
   }
 
-  static async removeTab(tabId: number) {
-    await chrome.tabs.remove(tabId);
-  }
-
   static async getPrivateModeWindows(): Promise<browser.windows.Window[]> {
     return (await browser.windows.getAll()).filter((win) => win.incognito);
   }
@@ -172,47 +218,6 @@ export class BrowserApi {
     );
   }
 
-  static async focusWindow(windowId: number) {
-    await chrome.windows.update(windowId, { focused: true });
-  }
-
-  static async openBitwardenExtensionTab(relativeUrl: string, active = true) {
-    let url = relativeUrl;
-    if (!relativeUrl.includes("uilocation=tab")) {
-      const fullUrl = chrome.extension.getURL(relativeUrl);
-      const parsedUrl = new URL(fullUrl);
-      parsedUrl.searchParams.set("uilocation", "tab");
-      url = parsedUrl.toString();
-    }
-
-    const createdTab = await this.createNewTab(url, active);
-    this.focusWindow(createdTab.windowId);
-  }
-
-  static async closeBitwardenExtensionTab() {
-    const tabs = await BrowserApi.tabsQuery({
-      active: true,
-      title: "Bitwarden",
-      windowType: "normal",
-      currentWindow: true,
-    });
-
-    if (tabs.length === 0) {
-      return;
-    }
-
-    const tabToClose = tabs[tabs.length - 1];
-    BrowserApi.removeTab(tabToClose.id);
-  }
-
-  static createNewWindow(
-    url: string,
-    focused = true,
-    type: chrome.windows.createTypeEnum = "normal"
-  ) {
-    chrome.windows.create({ url, focused, type });
-  }
-
   // Keep track of all the events registered in a Safari popup so we can remove
   // them when the popup gets unloaded, otherwise we cause a memory leak
   private static registeredMessageListeners: any[] = [];
diff --git a/apps/browser/src/platform/popup/abstractions/browser-popout-window.service.ts b/apps/browser/src/platform/popup/abstractions/browser-popout-window.service.ts
deleted file mode 100644
index f48649c4f23..00000000000
--- a/apps/browser/src/platform/popup/abstractions/browser-popout-window.service.ts
+++ /dev/null
@@ -1,42 +0,0 @@
-import { CipherType } from "@bitwarden/common/vault/enums/cipher-type";
-
-interface BrowserPopoutWindowService {
-  openUnlockPrompt(senderWindowId: number): Promise<void>;
-  closeUnlockPrompt(): Promise<void>;
-  openPasswordRepromptPrompt(
-    senderWindowId: number,
-    promptData: {
-      action: string;
-      cipherId: string;
-      senderTabId: number;
-    }
-  ): Promise<void>;
-  openCipherCreation(
-    senderWindowId: number,
-    promptData: {
-      cipherType?: CipherType;
-      senderTabId: number;
-      senderTabURI: string;
-    }
-  ): Promise<void>;
-  openCipherEdit(
-    senderWindowId: number,
-    promptData: {
-      cipherId: string;
-      senderTabId: number;
-      senderTabURI: string;
-    }
-  ): Promise<void>;
-  closePasswordRepromptPrompt(): Promise<void>;
-  openFido2Popout(
-    senderWindow: chrome.tabs.Tab,
-    promptData: {
-      sessionId: string;
-      senderTabId: number;
-      fallbackSupported: boolean;
-    }
-  ): Promise<number>;
-  closeFido2Popout(): Promise<void>;
-}
-
-export { BrowserPopoutWindowService };
diff --git a/apps/browser/src/platform/popup/abstractions/browser-popup-utils.abstractions.ts b/apps/browser/src/platform/popup/abstractions/browser-popup-utils.abstractions.ts
new file mode 100644
index 00000000000..c9952342e42
--- /dev/null
+++ b/apps/browser/src/platform/popup/abstractions/browser-popup-utils.abstractions.ts
@@ -0,0 +1,6 @@
+type ScrollOptions = {
+  delay: number;
+  containerSelector: string;
+};
+
+export { ScrollOptions };
diff --git a/apps/browser/src/platform/popup/browser-popout-window.service.ts b/apps/browser/src/platform/popup/browser-popout-window.service.ts
deleted file mode 100644
index c0ebcff6704..00000000000
--- a/apps/browser/src/platform/popup/browser-popout-window.service.ts
+++ /dev/null
@@ -1,174 +0,0 @@
-import { CipherType } from "@bitwarden/common/vault/enums/cipher-type";
-
-import { BrowserApi } from "../browser/browser-api";
-
-import { BrowserPopoutWindowService as BrowserPopupWindowServiceInterface } from "./abstractions/browser-popout-window.service";
-
-class BrowserPopoutWindowService implements BrowserPopupWindowServiceInterface {
-  private singleActionPopoutTabIds: Record<string, number> = {};
-  private defaultPopoutWindowOptions: chrome.windows.CreateData = {
-    type: "popup",
-    focused: true,
-    width: 380,
-    height: 630,
-  };
-
-  async openUnlockPrompt(senderWindowId: number) {
-    await this.openSingleActionPopout(
-      senderWindowId,
-      "popup/index.html?uilocation=popout",
-      "unlockPrompt"
-    );
-  }
-
-  async closeUnlockPrompt() {
-    await this.closeSingleActionPopout("unlockPrompt");
-  }
-
-  async openPasswordRepromptPrompt(
-    senderWindowId: number,
-    {
-      cipherId,
-      senderTabId,
-      action,
-    }: {
-      cipherId: string;
-      senderTabId: number;
-      action: string;
-    }
-  ) {
-    const promptWindowPath =
-      "popup/index.html#/view-cipher" +
-      "?uilocation=popout" +
-      `&cipherId=${cipherId}` +
-      `&senderTabId=${senderTabId}` +
-      `&action=${action}`;
-
-    await this.openSingleActionPopout(senderWindowId, promptWindowPath, "passwordReprompt");
-  }
-
-  async openCipherCreation(
-    senderWindowId: number,
-    {
-      cipherType = CipherType.Login,
-      senderTabId,
-      senderTabURI,
-    }: {
-      cipherType?: CipherType;
-      senderTabId: number;
-      senderTabURI: string;
-    }
-  ) {
-    const promptWindowPath =
-      "popup/index.html#/edit-cipher" +
-      "?uilocation=popout" +
-      `&type=${cipherType}` +
-      `&senderTabId=${senderTabId}` +
-      `&uri=${senderTabURI}`;
-
-    await this.openSingleActionPopout(senderWindowId, promptWindowPath, "cipherCreation");
-  }
-
-  async openCipherEdit(
-    senderWindowId: number,
-    {
-      cipherId,
-      senderTabId,
-      senderTabURI,
-    }: {
-      cipherId: string;
-      senderTabId: number;
-      senderTabURI: string;
-    }
-  ) {
-    const promptWindowPath =
-      "popup/index.html#/edit-cipher" +
-      "?uilocation=popout" +
-      `&cipherId=${cipherId}` +
-      `&senderTabId=${senderTabId}` +
-      `&uri=${senderTabURI}`;
-
-    await this.openSingleActionPopout(senderWindowId, promptWindowPath, "cipherEdit");
-  }
-
-  async closePasswordRepromptPrompt() {
-    await this.closeSingleActionPopout("passwordReprompt");
-  }
-
-  async openFido2Popout(
-    senderWindow: chrome.tabs.Tab,
-    {
-      sessionId,
-      senderTabId,
-      fallbackSupported,
-    }: {
-      sessionId: string;
-      senderTabId: number;
-      fallbackSupported: boolean;
-    }
-  ): Promise<number> {
-    await this.closeFido2Popout();
-
-    const promptWindowPath =
-      "popup/index.html#/fido2" +
-      "?uilocation=popout" +
-      `&sessionId=${sessionId}` +
-      `&fallbackSupported=${fallbackSupported}` +
-      `&senderTabId=${senderTabId}` +
-      `&senderUrl=${encodeURIComponent(senderWindow.url)}`;
-
-    return await this.openSingleActionPopout(
-      senderWindow.windowId,
-      promptWindowPath,
-      "fido2Popout",
-      {
-        height: 450,
-      }
-    );
-  }
-
-  async closeFido2Popout(): Promise<void> {
-    await this.closeSingleActionPopout("fido2Popout");
-  }
-
-  private async openSingleActionPopout(
-    senderWindowId: number,
-    popupWindowURL: string,
-    singleActionPopoutKey: string,
-    options: chrome.windows.CreateData = {}
-  ): Promise<number> {
-    const senderWindow = senderWindowId && (await BrowserApi.getWindow(senderWindowId));
-    const url = chrome.extension.getURL(popupWindowURL);
-    const offsetRight = 15;
-    const offsetTop = 90;
-    /// Use overrides in `options` if provided, otherwise use default
-    const popupWidth = options?.width || this.defaultPopoutWindowOptions.width;
-    const windowOptions = senderWindow
-      ? {
-          ...this.defaultPopoutWindowOptions,
-          left: senderWindow.left + senderWindow.width - popupWidth - offsetRight,
-          top: senderWindow.top + offsetTop,
-          ...options,
-          url,
-        }
-      : { ...this.defaultPopoutWindowOptions, url, ...options };
-
-    const popupWindow = await BrowserApi.createWindow(windowOptions);
-
-    await this.closeSingleActionPopout(singleActionPopoutKey);
-    this.singleActionPopoutTabIds[singleActionPopoutKey] = popupWindow?.tabs[0].id;
-
-    return popupWindow.id;
-  }
-
-  private async closeSingleActionPopout(popoutKey: string) {
-    const tabId = this.singleActionPopoutTabIds[popoutKey];
-
-    if (tabId) {
-      await BrowserApi.removeTab(tabId);
-    }
-    this.singleActionPopoutTabIds[popoutKey] = null;
-  }
-}
-
-export default BrowserPopoutWindowService;
diff --git a/apps/browser/src/platform/popup/browser-popup-utils.spec.ts b/apps/browser/src/platform/popup/browser-popup-utils.spec.ts
new file mode 100644
index 00000000000..7a9136ff9eb
--- /dev/null
+++ b/apps/browser/src/platform/popup/browser-popup-utils.spec.ts
@@ -0,0 +1,448 @@
+import { createChromeTabMock } from "../../autofill/jest/autofill-mocks";
+import { BrowserApi } from "../browser/browser-api";
+
+import BrowserPopupUtils from "./browser-popup-utils";
+
+describe("BrowserPopupUtils", () => {
+  afterEach(() => {
+    jest.clearAllMocks();
+  });
+
+  describe("inSidebar", () => {
+    it("should return true if the window contains the sidebar query param", () => {
+      const win = { location: { href: "https://jest-testing.com?uilocation=sidebar" } } as Window;
+
+      expect(BrowserPopupUtils.inSidebar(win)).toBe(true);
+    });
+
+    it("should return false if the window does not contain the sidebar query param", () => {
+      const win = { location: { href: "https://jest-testing.com?uilocation=popout" } } as Window;
+
+      expect(BrowserPopupUtils.inSidebar(win)).toBe(false);
+    });
+  });
+
+  describe("inPopout", () => {
+    it("should return true if the window contains the popout query param", () => {
+      const win = { location: { href: "https://jest-testing.com?uilocation=popout" } } as Window;
+
+      expect(BrowserPopupUtils.inPopout(win)).toBe(true);
+    });
+
+    it("should return false if the window does not contain the popout query param", () => {
+      const win = { location: { href: "https://jest-testing.com?uilocation=sidebar" } } as Window;
+
+      expect(BrowserPopupUtils.inPopout(win)).toBe(false);
+    });
+  });
+
+  describe("inSingleActionPopout", () => {
+    it("should return true if the window contains the singleActionPopout query param", () => {
+      const win = {
+        location: { href: "https://jest-testing.com?singleActionPopout=123" },
+      } as Window;
+
+      expect(BrowserPopupUtils.inSingleActionPopout(win, "123")).toBe(true);
+    });
+
+    it("should return false if the window does not contain the singleActionPopout query param", () => {
+      const win = { location: { href: "https://jest-testing.com" } } as Window;
+
+      expect(BrowserPopupUtils.inSingleActionPopout(win, "123")).toBe(false);
+    });
+  });
+
+  describe("inPopup", () => {
+    it("should return true if the window does not contain the popup query param", () => {
+      const win = { location: { href: "https://jest-testing.com" } } as Window;
+
+      expect(BrowserPopupUtils.inPopup(win)).toBe(true);
+    });
+
+    it("should return true if the window contains the popup query param", () => {
+      const win = { location: { href: "https://jest-testing.com?uilocation=popup" } } as Window;
+
+      expect(BrowserPopupUtils.inPopup(win)).toBe(true);
+    });
+
+    it("should return false if the window does not contain the popup query param", () => {
+      const win = { location: { href: "https://jest-testing.com?uilocation=sidebar" } } as Window;
+
+      expect(BrowserPopupUtils.inPopup(win)).toBe(false);
+    });
+  });
+
+  describe("getContentScrollY", () => {
+    it("should return the scroll position of the popup", () => {
+      const win = {
+        document: { getElementsByTagName: () => [{ scrollTop: 100 }] },
+      } as unknown as Window;
+
+      expect(BrowserPopupUtils.getContentScrollY(win)).toBe(100);
+    });
+  });
+
+  describe("setContentScrollY", () => {
+    it("should set the scroll position of the popup", async () => {
+      window.document.body.innerHTML = `
+        <main>
+          <div></div>
+        </main>
+      `;
+
+      await BrowserPopupUtils.setContentScrollY(window, 200);
+
+      expect(window.document.getElementsByTagName("main")[0].scrollTop).toBe(200);
+    });
+
+    it("should not set the scroll position of the popup if the scrollY is null", async () => {
+      window.document.body.innerHTML = `
+        <main>
+          <div></div>
+        </main>
+      `;
+
+      await BrowserPopupUtils.setContentScrollY(window, null);
+
+      expect(window.document.getElementsByTagName("main")[0].scrollTop).toBe(0);
+    });
+
+    it("will set the scroll position of the popup after the provided delay", async () => {
+      jest.useRealTimers();
+      window.document.body.innerHTML = `
+        <div class="scrolling-container">
+          <div></div>
+        </div>
+      `;
+
+      await BrowserPopupUtils.setContentScrollY(window, 300, {
+        delay: 200,
+        containerSelector: ".scrolling-container",
+      });
+
+      expect(window.document.querySelector(".scrolling-container").scrollTop).toBe(300);
+    });
+  });
+
+  describe("backgroundInitializationRequired", () => {
+    it("return true if the background page is a null value", () => {
+      jest.spyOn(BrowserApi, "getBackgroundPage").mockReturnValue(null);
+
+      expect(BrowserPopupUtils.backgroundInitializationRequired()).toBe(true);
+    });
+
+    it("return false if the background page is not a null value", () => {
+      jest.spyOn(BrowserApi, "getBackgroundPage").mockReturnValue({});
+
+      expect(BrowserPopupUtils.backgroundInitializationRequired()).toBe(false);
+    });
+  });
+
+  describe("inPrivateMode", () => {
+    it("returns false if the background requires initialization", () => {
+      jest.spyOn(BrowserPopupUtils, "backgroundInitializationRequired").mockReturnValue(false);
+
+      expect(BrowserPopupUtils.inPrivateMode()).toBe(false);
+    });
+
+    it("returns false if the manifest version is for version 3", () => {
+      jest.spyOn(BrowserPopupUtils, "backgroundInitializationRequired").mockReturnValue(true);
+      jest.spyOn(BrowserApi, "manifestVersion", "get").mockReturnValue(3);
+
+      expect(BrowserPopupUtils.inPrivateMode()).toBe(false);
+    });
+
+    it("returns true if the background does not require initalization and the manifest version is version 2", () => {
+      jest.spyOn(BrowserPopupUtils, "backgroundInitializationRequired").mockReturnValue(true);
+      jest.spyOn(BrowserApi, "manifestVersion", "get").mockReturnValue(2);
+
+      expect(BrowserPopupUtils.inPrivateMode()).toBe(true);
+    });
+  });
+
+  describe("openPopout", () => {
+    beforeEach(() => {
+      jest.spyOn(BrowserApi, "getWindow").mockResolvedValueOnce({
+        id: 1,
+        left: 100,
+        top: 100,
+        focused: false,
+        alwaysOnTop: false,
+        incognito: false,
+        width: 380,
+      });
+      jest.spyOn(BrowserApi, "createWindow").mockImplementation();
+    });
+
+    it("creates a window with the default window options", async () => {
+      const url = "popup/index.html";
+      jest.spyOn(BrowserPopupUtils as any, "isSingleActionPopoutOpen").mockResolvedValueOnce(false);
+
+      await BrowserPopupUtils.openPopout(url);
+
+      expect(BrowserApi.createWindow).toHaveBeenCalledWith({
+        type: "popup",
+        focused: true,
+        width: 380,
+        height: 630,
+        left: 85,
+        top: 190,
+        url: `chrome-extension://id/${url}?uilocation=popout`,
+      });
+    });
+
+    it("replaces any existing `uilocation=` query params within the passed extension url path to state the the uilocaiton is a popup", async () => {
+      const url = "popup/index.html#/tabs/vault?uilocation=sidebar";
+      jest.spyOn(BrowserPopupUtils as any, "isSingleActionPopoutOpen").mockResolvedValueOnce(false);
+
+      await BrowserPopupUtils.openPopout(url);
+
+      expect(BrowserApi.createWindow).toHaveBeenCalledWith({
+        type: "popup",
+        focused: true,
+        width: 380,
+        height: 630,
+        left: 85,
+        top: 190,
+        url: `chrome-extension://id/popup/index.html#/tabs/vault?uilocation=popout`,
+      });
+    });
+
+    it("appends the uilocation to the search params if an existing param is passed with the extension url path", async () => {
+      const url = "popup/index.html#/tabs/vault?existingParam=123";
+      jest.spyOn(BrowserPopupUtils as any, "isSingleActionPopoutOpen").mockResolvedValueOnce(false);
+
+      await BrowserPopupUtils.openPopout(url);
+
+      expect(BrowserApi.createWindow).toHaveBeenCalledWith({
+        type: "popup",
+        focused: true,
+        width: 380,
+        height: 630,
+        left: 85,
+        top: 190,
+        url: `chrome-extension://id/${url}&uilocation=popout`,
+      });
+    });
+
+    it("creates a single action popout window", async () => {
+      const url = "popup/index.html";
+      jest.spyOn(BrowserPopupUtils as any, "isSingleActionPopoutOpen").mockResolvedValueOnce(false);
+
+      await BrowserPopupUtils.openPopout(url, { singleActionKey: "123" });
+
+      expect(BrowserApi.createWindow).toHaveBeenCalledWith({
+        type: "popup",
+        focused: true,
+        width: 380,
+        height: 630,
+        left: 85,
+        top: 190,
+        url: `chrome-extension://id/${url}?uilocation=popout&singleActionPopout=123`,
+      });
+    });
+
+    it("does not create a single action popout window if it is already open", async () => {
+      const url = "popup/index.html";
+      jest.spyOn(BrowserPopupUtils as any, "isSingleActionPopoutOpen").mockResolvedValueOnce(true);
+
+      await BrowserPopupUtils.openPopout(url, { singleActionKey: "123" });
+
+      expect(BrowserApi.createWindow).not.toHaveBeenCalled();
+    });
+
+    it("creates a window with the provided window options", async () => {
+      const url = "popup/index.html";
+      jest.spyOn(BrowserPopupUtils as any, "isSingleActionPopoutOpen").mockResolvedValueOnce(false);
+
+      await BrowserPopupUtils.openPopout(url, {
+        windowOptions: {
+          type: "popup",
+          focused: false,
+          width: 100,
+          height: 100,
+        },
+      });
+
+      expect(BrowserApi.createWindow).toHaveBeenCalledWith({
+        type: "popup",
+        focused: false,
+        width: 100,
+        height: 100,
+        left: 85,
+        top: 190,
+        url: `chrome-extension://id/${url}?uilocation=popout`,
+      });
+    });
+
+    it("opens a single action window if the forceCloseExistingWindows param is true", async () => {
+      const url = "popup/index.html";
+      jest.spyOn(BrowserPopupUtils as any, "isSingleActionPopoutOpen").mockResolvedValueOnce(true);
+
+      await BrowserPopupUtils.openPopout(url, {
+        singleActionKey: "123",
+        forceCloseExistingWindows: true,
+      });
+
+      expect(BrowserApi.createWindow).toHaveBeenCalledWith({
+        type: "popup",
+        focused: true,
+        width: 380,
+        height: 630,
+        left: 85,
+        top: 190,
+        url: `chrome-extension://id/${url}?uilocation=popout&singleActionPopout=123`,
+      });
+    });
+  });
+
+  describe("openCurrentPagePopout", () => {
+    it("opens a popout window for the current page", async () => {
+      const win = { location: { href: "https://example.com#/tabs/current" } } as Window;
+      jest.spyOn(BrowserPopupUtils, "openPopout").mockImplementation();
+      jest.spyOn(BrowserApi, "closePopup").mockImplementation();
+      jest.spyOn(BrowserPopupUtils, "inPopup").mockReturnValue(false);
+
+      await BrowserPopupUtils.openCurrentPagePopout(win);
+
+      expect(BrowserPopupUtils.openPopout).toHaveBeenCalledWith("/#/tabs/vault");
+      expect(BrowserApi.closePopup).not.toHaveBeenCalled();
+    });
+
+    it("opens a popout window for the specified URL", async () => {
+      const win = {} as Window;
+      jest.spyOn(BrowserPopupUtils, "openPopout").mockImplementation();
+      jest.spyOn(BrowserPopupUtils, "inPopup").mockReturnValue(false);
+
+      await BrowserPopupUtils.openCurrentPagePopout(win, "https://example.com#/settings");
+
+      expect(BrowserPopupUtils.openPopout).toHaveBeenCalledWith("/#/settings");
+    });
+
+    it("opens a popout window for the current page and closes the popup window", async () => {
+      const win = { location: { href: "https://example.com/#/tabs/vault" } } as Window;
+      jest.spyOn(BrowserPopupUtils, "openPopout").mockImplementation();
+      jest.spyOn(BrowserApi, "closePopup").mockImplementation();
+      jest.spyOn(BrowserPopupUtils, "inPopup").mockReturnValue(true);
+
+      await BrowserPopupUtils.openCurrentPagePopout(win);
+
+      expect(BrowserPopupUtils.openPopout).toHaveBeenCalledWith("/#/tabs/vault");
+      expect(BrowserApi.closePopup).toHaveBeenCalledWith(win);
+    });
+  });
+
+  describe("closeSingleActionPopout", () => {
+    it("closes any existing single action popouts", async () => {
+      const url = "popup/index.html";
+      jest.useFakeTimers();
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValueOnce([
+        createChromeTabMock({
+          id: 10,
+          url: `chrome-extension://id/${url}?uilocation=popout&singleActionPopout=123`,
+          windowId: 11,
+        }),
+        createChromeTabMock({
+          id: 20,
+          url: `chrome-extension://id/${url}?uilocation=popout&singleActionPopout=123`,
+          windowId: 21,
+        }),
+        createChromeTabMock({
+          id: 30,
+          url: `chrome-extension://id/${url}?uilocation=popout&singleActionPopout=456`,
+          windowId: 31,
+        }),
+      ]);
+      jest.spyOn(BrowserApi, "removeWindow").mockResolvedValueOnce();
+
+      await BrowserPopupUtils.closeSingleActionPopout("123");
+      jest.runOnlyPendingTimers();
+
+      expect(BrowserApi.removeWindow).toHaveBeenNthCalledWith(1, 11);
+      expect(BrowserApi.removeWindow).toHaveBeenNthCalledWith(2, 21);
+      expect(BrowserApi.removeWindow).not.toHaveBeenCalledWith(31);
+    });
+  });
+
+  describe("isSingleActionPopoutOpen", () => {
+    const windowOptions = {
+      id: 1,
+      left: 100,
+      top: 100,
+      focused: false,
+      alwaysOnTop: false,
+      incognito: false,
+      width: 500,
+      height: 800,
+    };
+
+    beforeEach(() => {
+      jest.spyOn(BrowserApi, "updateWindowProperties").mockImplementation();
+      jest.spyOn(BrowserApi, "removeWindow").mockImplementation();
+    });
+
+    it("returns false if the popoutKey is not provided", async () => {
+      await expect(BrowserPopupUtils["isSingleActionPopoutOpen"](undefined, {})).resolves.toBe(
+        false
+      );
+    });
+
+    it("returns false if no popout windows are found", async () => {
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValueOnce([]);
+
+      await expect(
+        BrowserPopupUtils["isSingleActionPopoutOpen"]("123", windowOptions)
+      ).resolves.toBe(false);
+    });
+
+    it("returns false if no single action popout is found relating to the popoutKey", async () => {
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValueOnce([
+        createChromeTabMock({
+          id: 10,
+          url: `chrome-extension://id/popup/index.html?uilocation=popout&singleActionPopout=123`,
+        }),
+        createChromeTabMock({
+          id: 20,
+          url: `chrome-extension://id/popup/index.html?uilocation=popout&singleActionPopout=123`,
+        }),
+        createChromeTabMock({
+          id: 30,
+          url: `chrome-extension://id/popup/index.html?uilocation=popout&singleActionPopout=456`,
+        }),
+      ]);
+
+      await expect(
+        BrowserPopupUtils["isSingleActionPopoutOpen"]("789", windowOptions)
+      ).resolves.toBe(false);
+    });
+
+    it("returns true if a single action popout is found relating to the popoutKey", async () => {
+      jest.spyOn(BrowserApi, "tabsQuery").mockResolvedValueOnce([
+        createChromeTabMock({
+          id: 10,
+          url: `chrome-extension://id/popup/index.html?uilocation=popout&singleActionPopout=123`,
+        }),
+        createChromeTabMock({
+          id: 20,
+          url: `chrome-extension://id/popup/index.html?uilocation=popout&singleActionPopout=123`,
+        }),
+        createChromeTabMock({
+          id: 30,
+          url: `chrome-extension://id/popup/index.html?uilocation=popout&singleActionPopout=456`,
+        }),
+      ]);
+
+      await expect(
+        BrowserPopupUtils["isSingleActionPopoutOpen"]("123", windowOptions)
+      ).resolves.toBe(true);
+      expect(BrowserApi.updateWindowProperties).toHaveBeenCalledWith(2, {
+        focused: true,
+        width: 500,
+        height: 800,
+        top: 100,
+        left: 100,
+      });
+      expect(BrowserApi.removeWindow).toHaveBeenCalledTimes(1);
+    });
+  });
+});
diff --git a/apps/browser/src/platform/popup/browser-popup-utils.ts b/apps/browser/src/platform/popup/browser-popup-utils.ts
new file mode 100644
index 00000000000..3e687fa0815
--- /dev/null
+++ b/apps/browser/src/platform/popup/browser-popup-utils.ts
@@ -0,0 +1,275 @@
+import { BrowserApi } from "../browser/browser-api";
+
+import { ScrollOptions } from "./abstractions/browser-popup-utils.abstractions";
+
+class BrowserPopupUtils {
+  /**
+   * Identifies if the popup is within the sidebar.
+   *
+   * @param win - The passed window object.
+   */
+  static inSidebar(win: Window): boolean {
+    return BrowserPopupUtils.urlContainsSearchParams(win, "uilocation", "sidebar");
+  }
+
+  /**
+   * Identifies if the popup is within the popout.
+   *
+   * @param win - The passed window object.
+   */
+  static inPopout(win: Window): boolean {
+    return BrowserPopupUtils.urlContainsSearchParams(win, "uilocation", "popout");
+  }
+
+  /**
+   * Identifies if the popup is within the single action popout.
+   *
+   * @param win - The passed window object.
+   * @param popoutKey - The single action popout key used to identify the popout.
+   */
+  static inSingleActionPopout(win: Window, popoutKey: string): boolean {
+    return BrowserPopupUtils.urlContainsSearchParams(win, "singleActionPopout", popoutKey);
+  }
+
+  /**
+   * Identifies if the popup is within the popup.
+   *
+   * @param win - The passed window object.
+   */
+  static inPopup(win: Window): boolean {
+    return (
+      win.location.href.indexOf("uilocation=") === -1 ||
+      win.location.href.indexOf("uilocation=popup") > -1
+    );
+  }
+
+  /**
+   * Gets the scroll position of the popup.
+   *
+   * @param win - The passed window object.
+   * @param scrollingContainer - Element tag name of the scrolling container.
+   */
+  static getContentScrollY(win: Window, scrollingContainer = "main"): number {
+    const content = win.document.getElementsByTagName(scrollingContainer)[0];
+    return content.scrollTop;
+  }
+
+  /**
+   * Sets the scroll position of the popup.
+   *
+   * @param win - The passed window object.
+   * @param scrollYAmount - The amount to scroll the popup.
+   * @param options - Allows for setting the delay in ms to wait before scrolling the popup and the scrolling container tag name.
+   */
+  static async setContentScrollY(
+    win: Window,
+    scrollYAmount: number | undefined,
+    options: ScrollOptions = {
+      delay: 0,
+      containerSelector: "main",
+    }
+  ) {
+    const { delay, containerSelector } = options;
+    return new Promise<void>((resolve) =>
+      win.setTimeout(() => {
+        const container = win.document.querySelector(containerSelector);
+        if (!isNaN(scrollYAmount) && container) {
+          container.scrollTop = scrollYAmount;
+        }
+
+        resolve();
+      }, delay)
+    );
+  }
+
+  /**
+   * Identifies if the background page needs to be initialized.
+   */
+  static backgroundInitializationRequired() {
+    return BrowserApi.getBackgroundPage() === null;
+  }
+
+  /**
+   * Identifies if the popup is loading in private mode.
+   */
+  static inPrivateMode() {
+    return BrowserPopupUtils.backgroundInitializationRequired() && BrowserApi.manifestVersion !== 3;
+  }
+
+  /**
+   * Opens a popout window of any extension page. If the popout window is already open, it will be focused.
+   *
+   * @param extensionUrlPath - A relative path to the extension page. Example: "popup/index.html#/tabs/vault"
+   * @param options - Options for the popout window that overrides the default options.
+   */
+  static async openPopout(
+    extensionUrlPath: string,
+    options: {
+      senderWindowId?: number;
+      singleActionKey?: string;
+      forceCloseExistingWindows?: boolean;
+      windowOptions?: Partial<chrome.windows.CreateData>;
+    } = {}
+  ) {
+    const { senderWindowId, singleActionKey, forceCloseExistingWindows, windowOptions } = options;
+    const defaultPopoutWindowOptions: chrome.windows.CreateData = {
+      type: "popup",
+      focused: true,
+      width: 380,
+      height: 630,
+    };
+    const offsetRight = 15;
+    const offsetTop = 90;
+    const popupWidth = defaultPopoutWindowOptions.width;
+    const senderWindow = await BrowserApi.getWindow(senderWindowId);
+    const popoutWindowOptions = {
+      left: senderWindow.left + senderWindow.width - popupWidth - offsetRight,
+      top: senderWindow.top + offsetTop,
+      ...defaultPopoutWindowOptions,
+      ...windowOptions,
+      url: chrome.runtime.getURL(
+        BrowserPopupUtils.buildPopoutUrlPath(extensionUrlPath, singleActionKey)
+      ),
+    };
+
+    if (
+      (await BrowserPopupUtils.isSingleActionPopoutOpen(
+        singleActionKey,
+        popoutWindowOptions,
+        forceCloseExistingWindows
+      )) &&
+      !forceCloseExistingWindows
+    ) {
+      return;
+    }
+
+    return await BrowserApi.createWindow(popoutWindowOptions);
+  }
+
+  /**
+   * Closes the single action popout window.
+   *
+   * @param popoutKey - The single action popout key used to identify the popout.
+   * @param delayClose - The amount of time to wait before closing the popout. Defaults to 0.
+   */
+  static async closeSingleActionPopout(popoutKey: string, delayClose = 0): Promise<void> {
+    const extensionUrl = chrome.runtime.getURL("popup/index.html");
+    const tabs = await BrowserApi.tabsQuery({ url: `${extensionUrl}*` });
+    for (const tab of tabs) {
+      if (!tab.url.includes(`singleActionPopout=${popoutKey}`)) {
+        continue;
+      }
+
+      setTimeout(() => BrowserApi.removeWindow(tab.windowId), delayClose);
+    }
+  }
+
+  /**
+   * Opens a popout window for the current page.
+   * If the current page is set for the current tab, then the
+   * popout window will be set for the vault items listing tab.
+   *
+   * @param win - The passed window object.
+   * @param href - The href to open in the popout window.
+   */
+  static async openCurrentPagePopout(win: Window, href: string = null) {
+    const popoutUrl = href || win.location.href;
+    const parsedUrl = new URL(popoutUrl);
+    let hashRoute = parsedUrl.hash;
+    if (hashRoute.startsWith("#/tabs/current")) {
+      hashRoute = "#/tabs/vault";
+    }
+
+    await BrowserPopupUtils.openPopout(`${parsedUrl.pathname}${hashRoute}`);
+
+    if (BrowserPopupUtils.inPopup(win)) {
+      BrowserApi.closePopup(win);
+    }
+  }
+
+  /**
+   * Identifies if a single action window is open based on the passed popoutKey.
+   * Will focus the existing window, and close any other windows that might exist
+   * with the same popout key.
+   *
+   * @param popoutKey - The single action popout key used to identify the popout.
+   * @param windowInfo - The window info to use to update the existing window.
+   * @param forceCloseExistingWindows - Identifies if the existing windows should be closed.
+   */
+  private static async isSingleActionPopoutOpen(
+    popoutKey: string | undefined,
+    windowInfo: chrome.windows.CreateData,
+    forceCloseExistingWindows = false
+  ) {
+    if (!popoutKey) {
+      return false;
+    }
+
+    const extensionUrl = chrome.runtime.getURL("popup/index.html");
+    const popoutTabs = (await BrowserApi.tabsQuery({ url: `${extensionUrl}*` })).filter((tab) =>
+      tab.url.includes(`singleActionPopout=${popoutKey}`)
+    );
+    if (popoutTabs.length === 0) {
+      return false;
+    }
+
+    if (!forceCloseExistingWindows) {
+      // Update first, remove it from list
+      const tab = popoutTabs.shift();
+      await BrowserApi.updateWindowProperties(tab.windowId, {
+        focused: true,
+        width: windowInfo.width,
+        height: windowInfo.height,
+        top: windowInfo.top,
+        left: windowInfo.left,
+      });
+    }
+
+    popoutTabs.forEach((tab) => BrowserApi.removeWindow(tab.windowId));
+
+    return true;
+  }
+
+  /**
+   * Identifies if the url contains the specified search param and value.
+   *
+   * @param win - The passed window object.
+   * @param searchParam - The search param to identify.
+   * @param searchValue - The search value to identify.
+   */
+  private static urlContainsSearchParams(
+    win: Window,
+    searchParam: string,
+    searchValue: string
+  ): boolean {
+    return win.location.href.indexOf(`${searchParam}=${searchValue}`) > -1;
+  }
+
+  /**
+   * Builds the popout url path. Ensures that the uilocation param is set to
+   * `popout` and that the singleActionPopout param is set to the passed singleActionKey.
+   *
+   * @param extensionUrlPath - A relative path to the extension page. Example: "popup/index.html#/tabs/vault"
+   * @param singleActionKey - The single action popout key used to identify the popout.
+   */
+  private static buildPopoutUrlPath(extensionUrlPath: string, singleActionKey: string) {
+    let formattedExtensionUrlPath = extensionUrlPath;
+    if (formattedExtensionUrlPath.includes("uilocation=")) {
+      formattedExtensionUrlPath = formattedExtensionUrlPath.replace(
+        /uilocation=[^&]*/g,
+        "uilocation=popout"
+      );
+    } else {
+      formattedExtensionUrlPath +=
+        (formattedExtensionUrlPath.includes("?") ? "&" : "?") + "uilocation=popout";
+    }
+
+    if (singleActionKey) {
+      formattedExtensionUrlPath += `&singleActionPopout=${singleActionKey}`;
+    }
+
+    return formattedExtensionUrlPath;
+  }
+}
+
+export default BrowserPopupUtils;
diff --git a/apps/browser/src/popup/components/pop-out.component.ts b/apps/browser/src/popup/components/pop-out.component.ts
index b8675ec4d4c..88587574359 100644
--- a/apps/browser/src/popup/components/pop-out.component.ts
+++ b/apps/browser/src/popup/components/pop-out.component.ts
@@ -2,7 +2,7 @@ import { Component, Input, OnInit } from "@angular/core";
 
 import { PlatformUtilsService } from "@bitwarden/common/platform/abstractions/platform-utils.service";
 
-import { PopupUtilsService } from "../services/popup-utils.service";
+import BrowserPopupUtils from "../../platform/popup/browser-popup-utils";
 
 @Component({
   selector: "app-pop-out",
@@ -11,16 +11,13 @@ import { PopupUtilsService } from "../services/popup-utils.service";
 export class PopOutComponent implements OnInit {
   @Input() show = true;
 
-  constructor(
-    private platformUtilsService: PlatformUtilsService,
-    private popupUtilsService: PopupUtilsService
-  ) {}
+  constructor(private platformUtilsService: PlatformUtilsService) {}
 
   ngOnInit() {
     if (this.show) {
       if (
-        (this.popupUtilsService.inSidebar(window) && this.platformUtilsService.isFirefox()) ||
-        this.popupUtilsService.inPopout(window)
+        (BrowserPopupUtils.inSidebar(window) && this.platformUtilsService.isFirefox()) ||
+        BrowserPopupUtils.inPopout(window)
       ) {
         this.show = false;
       }
@@ -28,6 +25,6 @@ export class PopOutComponent implements OnInit {
   }
 
   expand() {
-    this.popupUtilsService.popOut(window);
+    BrowserPopupUtils.openCurrentPagePopout(window);
   }
 }
diff --git a/apps/browser/src/popup/components/private-mode-warning.component.ts b/apps/browser/src/popup/components/private-mode-warning.component.ts
index 4d5587d65f1..ff6292bdbf6 100644
--- a/apps/browser/src/popup/components/private-mode-warning.component.ts
+++ b/apps/browser/src/popup/components/private-mode-warning.component.ts
@@ -1,6 +1,6 @@
 import { Component, OnInit } from "@angular/core";
 
-import { PopupUtilsService } from "../services/popup-utils.service";
+import BrowserPopupUtils from "../../platform/popup/browser-popup-utils";
 
 @Component({
   selector: "app-private-mode-warning",
@@ -9,9 +9,7 @@ import { PopupUtilsService } from "../services/popup-utils.service";
 export class PrivateModeWarningComponent implements OnInit {
   showWarning = false;
 
-  constructor(private popupUtilsService: PopupUtilsService) {}
-
   ngOnInit() {
-    this.showWarning = this.popupUtilsService.inPrivateMode();
+    this.showWarning = BrowserPopupUtils.inPrivateMode();
   }
 }
diff --git a/apps/browser/src/popup/services/init.service.ts b/apps/browser/src/popup/services/init.service.ts
index c9a1ffb720e..5dd76ebe183 100644
--- a/apps/browser/src/popup/services/init.service.ts
+++ b/apps/browser/src/popup/services/init.service.ts
@@ -6,16 +6,14 @@ import { LogService as LogServiceAbstraction } from "@bitwarden/common/platform/
 import { PlatformUtilsService } from "@bitwarden/common/platform/abstractions/platform-utils.service";
 import { ConfigService } from "@bitwarden/common/platform/services/config/config.service";
 
+import BrowserPopupUtils from "../../platform/popup/browser-popup-utils";
 import { BrowserStateService as StateServiceAbstraction } from "../../platform/services/abstractions/browser-state.service";
 
-import { PopupUtilsService } from "./popup-utils.service";
-
 @Injectable()
 export class InitService {
   constructor(
     private platformUtilsService: PlatformUtilsService,
     private i18nService: I18nService,
-    private popupUtilsService: PopupUtilsService,
     private stateService: StateServiceAbstraction,
     private logService: LogServiceAbstraction,
     private themingService: AbstractThemingService,
@@ -26,7 +24,7 @@ export class InitService {
     return async () => {
       await this.stateService.init();
 
-      if (!this.popupUtilsService.inPopup(window)) {
+      if (!BrowserPopupUtils.inPopup(window)) {
         window.document.body.classList.add("body-full");
       } else if (window.screen.availHeight < 600) {
         window.document.body.classList.add("body-xs");
@@ -43,7 +41,7 @@ export class InitService {
       if (
         this.platformUtilsService.isChrome() &&
         navigator.platform.indexOf("Mac") > -1 &&
-        this.popupUtilsService.inPopup(window) &&
+        BrowserPopupUtils.inPopup(window) &&
         (window.screenLeft < 0 ||
           window.screenTop < 0 ||
           window.screenLeft > window.screen.width ||
diff --git a/apps/browser/src/popup/services/popup-close-warning.service.ts b/apps/browser/src/popup/services/popup-close-warning.service.ts
new file mode 100644
index 00000000000..536def47d5d
--- /dev/null
+++ b/apps/browser/src/popup/services/popup-close-warning.service.ts
@@ -0,0 +1,39 @@
+import { Injectable } from "@angular/core";
+import { fromEvent, Subscription } from "rxjs";
+
+@Injectable()
+export class PopupCloseWarningService {
+  private unloadSubscription: Subscription;
+
+  /**
+   * Enables a pop-up warning before the user exits the window/tab, or navigates away.
+   * This warns the user that they may lose unsaved data if they leave the page.
+   * (Note: navigating within the Angular app will not trigger it because it's an SPA.)
+   * Make sure you call `PopupCloseWarningService.disable` when it is no longer relevant.
+   */
+  enable() {
+    this.disable();
+
+    this.unloadSubscription = fromEvent(window, "beforeunload").subscribe(
+      (e: BeforeUnloadEvent) => {
+        // Recommended method but not widely supported
+        e.preventDefault();
+
+        // Modern browsers do not display this message, it just needs to be a non-nullish value
+        // Exact wording is determined by the browser
+        const confirmationMessage = "";
+
+        // Older methods with better support
+        e.returnValue = confirmationMessage;
+        return confirmationMessage;
+      }
+    );
+  }
+
+  /**
+   * Disables the warning enabled by PopupCloseWarningService.enable.
+   */
+  disable() {
+    this.unloadSubscription?.unsubscribe();
+  }
+}
diff --git a/apps/browser/src/popup/services/popup-utils.service.ts b/apps/browser/src/popup/services/popup-utils.service.ts
index b5a5a058171..e69de29bb2d 100644
--- a/apps/browser/src/popup/services/popup-utils.service.ts
+++ b/apps/browser/src/popup/services/popup-utils.service.ts
@@ -1,151 +0,0 @@
-import { Injectable } from "@angular/core";
-import { fromEvent, Subscription } from "rxjs";
-
-import { BrowserApi } from "../../platform/browser/browser-api";
-
-export type Popout =
-  | {
-      type: "window";
-      window: chrome.windows.Window;
-    }
-  | {
-      type: "tab";
-      tab: chrome.tabs.Tab;
-    };
-
-@Injectable()
-export class PopupUtilsService {
-  private unloadSubscription: Subscription;
-
-  constructor(private privateMode: boolean = false) {}
-
-  inSidebar(win: Window): boolean {
-    return win.location.search !== "" && win.location.search.indexOf("uilocation=sidebar") > -1;
-  }
-
-  inTab(win: Window): boolean {
-    return win.location.search !== "" && win.location.search.indexOf("uilocation=tab") > -1;
-  }
-
-  inPopout(win: Window): boolean {
-    return win.location.search !== "" && win.location.search.indexOf("uilocation=popout") > -1;
-  }
-
-  inPopup(win: Window): boolean {
-    return (
-      win.location.search === "" ||
-      win.location.search.indexOf("uilocation=") === -1 ||
-      win.location.search.indexOf("uilocation=popup") > -1
-    );
-  }
-
-  inPrivateMode(): boolean {
-    return this.privateMode;
-  }
-
-  getContentScrollY(win: Window, scrollingContainer = "main"): number {
-    const content = win.document.getElementsByTagName(scrollingContainer)[0];
-    return content.scrollTop;
-  }
-
-  setContentScrollY(win: Window, scrollY: number, scrollingContainer = "main"): void {
-    if (scrollY != null) {
-      const content = win.document.getElementsByTagName(scrollingContainer)[0];
-      content.scrollTop = scrollY;
-    }
-  }
-
-  async popOut(
-    win: Window,
-    href: string = null,
-    options: { center?: boolean } = {}
-  ): Promise<Popout> {
-    if (href === null) {
-      href = win.location.href;
-    }
-
-    if (typeof chrome !== "undefined" && chrome?.windows?.create != null) {
-      if (href.indexOf("?uilocation=") > -1) {
-        href = href
-          .replace("uilocation=popup", "uilocation=popout")
-          .replace("uilocation=tab", "uilocation=popout")
-          .replace("uilocation=sidebar", "uilocation=popout");
-      } else {
-        const hrefParts = href.split("#");
-        href =
-          hrefParts[0] + "?uilocation=popout" + (hrefParts.length > 0 ? "#" + hrefParts[1] : "");
-      }
-
-      const bodyRect = document.querySelector("body").getBoundingClientRect();
-      const width = Math.round(bodyRect.width ? bodyRect.width + 60 : 375);
-      const height = Math.round(bodyRect.height || 600);
-      const top = options.center ? Math.round((screen.height - height) / 2) : undefined;
-      const left = options.center ? Math.round((screen.width - width) / 2) : undefined;
-      const window = await BrowserApi.createWindow({
-        url: href,
-        type: "popup",
-        width,
-        height,
-        top,
-        left,
-      });
-
-      if (win && this.inPopup(win)) {
-        BrowserApi.closePopup(win);
-      }
-
-      return { type: "window", window };
-    } else if (chrome?.tabs?.create != null) {
-      href = href
-        .replace("uilocation=popup", "uilocation=tab")
-        .replace("uilocation=popout", "uilocation=tab")
-        .replace("uilocation=sidebar", "uilocation=tab");
-
-      const tab = await BrowserApi.createNewTab(href);
-      return { type: "tab", tab };
-    } else {
-      throw new Error("Cannot open tab or window");
-    }
-  }
-
-  closePopOut(popout: Popout): Promise<void> {
-    switch (popout.type) {
-      case "window":
-        return BrowserApi.removeWindow(popout.window.id);
-      case "tab":
-        return BrowserApi.removeTab(popout.tab.id);
-    }
-  }
-
-  /**
-   * Enables a pop-up warning before the user exits the window/tab, or navigates away.
-   * This warns the user that they may lose unsaved data if they leave the page.
-   * (Note: navigating within the Angular app will not trigger it because it's an SPA.)
-   * Make sure you call `disableTabCloseWarning` when it is no longer relevant.
-   */
-  enableCloseTabWarning() {
-    this.disableCloseTabWarning();
-
-    this.unloadSubscription = fromEvent(window, "beforeunload").subscribe(
-      (e: BeforeUnloadEvent) => {
-        // Recommended method but not widely supported
-        e.preventDefault();
-
-        // Modern browsers do not display this message, it just needs to be a non-nullish value
-        // Exact wording is determined by the browser
-        const confirmationMessage = "";
-
-        // Older methods with better support
-        e.returnValue = confirmationMessage;
-        return confirmationMessage;
-      }
-    );
-  }
-
-  /**
-   * Disables the warning enabled by enableCloseTabWarning.
-   */
-  disableCloseTabWarning() {
-    this.unloadSubscription?.unsubscribe();
-  }
-}
diff --git a/apps/browser/src/popup/services/services.module.ts b/apps/browser/src/popup/services/services.module.ts
index 2bdeaffc3d9..2edc90286b0 100644
--- a/apps/browser/src/popup/services/services.module.ts
+++ b/apps/browser/src/popup/services/services.module.ts
@@ -94,6 +94,7 @@ import { AutofillService } from "../../autofill/services/abstractions/autofill.s
 import MainBackground from "../../background/main.background";
 import { Account } from "../../models/account";
 import { BrowserApi } from "../../platform/browser/browser-api";
+import BrowserPopupUtils from "../../platform/popup/browser-popup-utils";
 import { BrowserStateService as StateServiceAbstraction } from "../../platform/services/abstractions/browser-state.service";
 import { BrowserConfigService } from "../../platform/services/browser-config.service";
 import { BrowserEnvironmentService } from "../../platform/services/browser-environment.service";
@@ -110,11 +111,11 @@ import { VaultFilterService } from "../../vault/services/vault-filter.service";
 
 import { DebounceNavigationService } from "./debounceNavigationService";
 import { InitService } from "./init.service";
+import { PopupCloseWarningService } from "./popup-close-warning.service";
 import { PopupSearchService } from "./popup-search.service";
-import { PopupUtilsService } from "./popup-utils.service";
 
-const needsBackgroundInit = BrowserApi.getBackgroundPage() == null;
-const isPrivateMode = needsBackgroundInit && BrowserApi.manifestVersion !== 3;
+const needsBackgroundInit = BrowserPopupUtils.backgroundInitializationRequired();
+const isPrivateMode = BrowserPopupUtils.inPrivateMode();
 const mainBackground: MainBackground = needsBackgroundInit
   ? createLocalBgService()
   : BrowserApi.getBackgroundPage().bitwardenMain;
@@ -138,6 +139,7 @@ function getBgService<T>(service: keyof MainBackground) {
     InitService,
     DebounceNavigationService,
     DialogService,
+    PopupCloseWarningService,
     {
       provide: LOCALE_ID,
       useFactory: () => getBgService<I18nServiceAbstraction>("i18nService")().translationLocale,
@@ -150,7 +152,6 @@ function getBgService<T>(service: keyof MainBackground) {
       multi: true,
     },
     { provide: BaseUnauthGuardService, useClass: UnauthGuardService },
-    { provide: PopupUtilsService, useFactory: () => new PopupUtilsService(isPrivateMode) },
     {
       provide: MessagingService,
       useFactory: () => {
@@ -523,13 +524,10 @@ function getBgService<T>(service: keyof MainBackground) {
     },
     {
       provide: FilePopoutUtilsService,
-      useFactory: (
-        platformUtilsService: PlatformUtilsService,
-        popupUtilsService: PopupUtilsService
-      ) => {
-        return new FilePopoutUtilsService(platformUtilsService, popupUtilsService);
+      useFactory: (platformUtilsService: PlatformUtilsService) => {
+        return new FilePopoutUtilsService(platformUtilsService);
       },
-      deps: [PlatformUtilsService, PopupUtilsService],
+      deps: [PlatformUtilsService],
     },
   ],
 })
diff --git a/apps/browser/src/popup/settings/settings.component.ts b/apps/browser/src/popup/settings/settings.component.ts
index 439402437e6..b67564a07b5 100644
--- a/apps/browser/src/popup/settings/settings.component.ts
+++ b/apps/browser/src/popup/settings/settings.component.ts
@@ -36,7 +36,7 @@ import { DialogService } from "@bitwarden/components";
 import { SetPinComponent } from "../../auth/popup/components/set-pin.component";
 import { BiometricErrors, BiometricErrorTypes } from "../../models/biometricErrors";
 import { BrowserApi } from "../../platform/browser/browser-api";
-import { PopupUtilsService } from "../services/popup-utils.service";
+import BrowserPopupUtils from "../../platform/popup/browser-popup-utils";
 
 import { AboutComponent } from "./about.component";
 import { AwaitDesktopDialogComponent } from "./await-desktop-dialog.component";
@@ -95,7 +95,6 @@ export class SettingsComponent implements OnInit {
     private environmentService: EnvironmentService,
     private cryptoService: CryptoService,
     private stateService: StateService,
-    private popupUtilsService: PopupUtilsService,
     private modalService: ModalService,
     private userVerificationService: UserVerificationService,
     private dialogService: DialogService,
@@ -335,7 +334,7 @@ export class SettingsComponent implements OnInit {
         // eslint-disable-next-line
         console.error(e);
 
-        if (this.platformUtilsService.isFirefox() && this.popupUtilsService.inSidebar(window)) {
+        if (this.platformUtilsService.isFirefox() && BrowserPopupUtils.inSidebar(window)) {
           await this.dialogService.openSimpleDialog({
             title: { key: "nativeMessaginPermissionSidebarTitle" },
             content: { key: "nativeMessaginPermissionSidebarDesc" },
@@ -474,7 +473,7 @@ export class SettingsComponent implements OnInit {
   async import() {
     await this.router.navigate(["/import"]);
     if (await BrowserApi.isPopupOpen()) {
-      this.popupUtilsService.popOut(window);
+      BrowserPopupUtils.openCurrentPagePopout(window);
     }
   }
 
diff --git a/apps/browser/src/popup/tabs.component.ts b/apps/browser/src/popup/tabs.component.ts
index 856529a0a3b..7546c9ca13b 100644
--- a/apps/browser/src/popup/tabs.component.ts
+++ b/apps/browser/src/popup/tabs.component.ts
@@ -1,6 +1,6 @@
 import { Component, OnInit } from "@angular/core";
 
-import { PopupUtilsService } from "./services/popup-utils.service";
+import BrowserPopupUtils from "../platform/popup/browser-popup-utils";
 
 @Component({
   selector: "app-tabs",
@@ -9,9 +9,7 @@ import { PopupUtilsService } from "./services/popup-utils.service";
 export class TabsComponent implements OnInit {
   showCurrentTab = true;
 
-  constructor(private popupUtilsService: PopupUtilsService) {}
-
   ngOnInit() {
-    this.showCurrentTab = !this.popupUtilsService.inPopout(window);
+    this.showCurrentTab = !BrowserPopupUtils.inPopout(window);
   }
 }
diff --git a/apps/browser/src/tools/popup/components/file-popout-callout.component.ts b/apps/browser/src/tools/popup/components/file-popout-callout.component.ts
index 2231b2ab595..eae0f12ad94 100644
--- a/apps/browser/src/tools/popup/components/file-popout-callout.component.ts
+++ b/apps/browser/src/tools/popup/components/file-popout-callout.component.ts
@@ -4,7 +4,7 @@ import { Component, OnInit } from "@angular/core";
 import { JslibModule } from "@bitwarden/angular/jslib.module";
 import { CalloutModule } from "@bitwarden/components";
 
-import { PopupUtilsService } from "../../../popup/services/popup-utils.service";
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
 import { FilePopoutUtilsService } from "../services/file-popout-utils.service";
 
 @Component({
@@ -19,10 +19,7 @@ export class FilePopoutCalloutComponent implements OnInit {
   protected showSafariFileWarning: boolean;
   protected showChromiumFileWarning: boolean;
 
-  constructor(
-    private popupUtilsService: PopupUtilsService,
-    private filePopoutUtilsService: FilePopoutUtilsService
-  ) {}
+  constructor(private filePopoutUtilsService: FilePopoutUtilsService) {}
 
   ngOnInit() {
     this.showFilePopoutMessage = this.filePopoutUtilsService.showFilePopoutMessage(window);
@@ -32,6 +29,6 @@ export class FilePopoutCalloutComponent implements OnInit {
   }
 
   popOutWindow() {
-    this.popupUtilsService.popOut(window);
+    BrowserPopupUtils.openCurrentPagePopout(window);
   }
 }
diff --git a/apps/browser/src/tools/popup/send/send-add-edit.component.ts b/apps/browser/src/tools/popup/send/send-add-edit.component.ts
index ae81779b08a..5ad664d871e 100644
--- a/apps/browser/src/tools/popup/send/send-add-edit.component.ts
+++ b/apps/browser/src/tools/popup/send/send-add-edit.component.ts
@@ -15,8 +15,8 @@ import { SendApiService } from "@bitwarden/common/tools/send/services/send-api.s
 import { SendService } from "@bitwarden/common/tools/send/services/send.service.abstraction";
 import { DialogService } from "@bitwarden/components";
 
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
 import { BrowserStateService } from "../../../platform/services/abstractions/browser-state.service";
-import { PopupUtilsService } from "../../../popup/services/popup-utils.service";
 import { FilePopoutUtilsService } from "../services/file-popout-utils.service";
 
 @Component({
@@ -44,7 +44,6 @@ export class SendAddEditComponent extends BaseAddEditComponent {
     private route: ActivatedRoute,
     private router: Router,
     private location: Location,
-    private popupUtilsService: PopupUtilsService,
     logService: LogService,
     sendApiService: SendApiService,
     dialogService: DialogService,
@@ -68,14 +67,14 @@ export class SendAddEditComponent extends BaseAddEditComponent {
   }
 
   popOutWindow() {
-    this.popupUtilsService.popOut(window);
+    BrowserPopupUtils.openCurrentPagePopout(window);
   }
 
   async ngOnInit() {
     // File visibility
     this.showFileSelector =
       !this.editMode && !this.filePopoutUtilsService.showFilePopoutMessage(window);
-    this.inPopout = this.popupUtilsService.inPopout(window);
+    this.inPopout = BrowserPopupUtils.inPopout(window);
     this.isFirefox = this.platformUtilsService.isFirefox();
 
     // eslint-disable-next-line rxjs-angular/prefer-takeuntil, rxjs/no-async-subscribe
diff --git a/apps/browser/src/tools/popup/send/send-groupings.component.ts b/apps/browser/src/tools/popup/send/send-groupings.component.ts
index e93064fe80b..0fde93df8fe 100644
--- a/apps/browser/src/tools/popup/send/send-groupings.component.ts
+++ b/apps/browser/src/tools/popup/send/send-groupings.component.ts
@@ -17,8 +17,8 @@ import { SyncService } from "@bitwarden/common/vault/abstractions/sync/sync.serv
 import { DialogService } from "@bitwarden/components";
 
 import { BrowserSendComponentState } from "../../../models/browserSendComponentState";
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
 import { BrowserStateService } from "../../../platform/services/abstractions/browser-state.service";
-import { PopupUtilsService } from "../../../popup/services/popup-utils.service";
 
 const ComponentId = "SendComponent";
 
@@ -43,7 +43,6 @@ export class SendGroupingsComponent extends BaseSendComponent {
     ngZone: NgZone,
     policyService: PolicyService,
     searchService: SearchService,
-    private popupUtils: PopupUtilsService,
     private stateService: BrowserStateService,
     private router: Router,
     private syncService: SyncService,
@@ -74,7 +73,7 @@ export class SendGroupingsComponent extends BaseSendComponent {
   async ngOnInit() {
     // Determine Header details
     this.showLeftHeader = !(
-      this.popupUtils.inSidebar(window) && this.platformUtilsService.isFirefox()
+      BrowserPopupUtils.inSidebar(window) && this.platformUtilsService.isFirefox()
     );
     // Clear state of Send Type Component
     await this.stateService.setBrowserSendTypeComponentState(null);
@@ -97,7 +96,7 @@ export class SendGroupingsComponent extends BaseSendComponent {
     }
 
     if (!this.syncService.syncInProgress || restoredScopeState) {
-      window.setTimeout(() => this.popupUtils.setContentScrollY(window, this.state?.scrollY), 0);
+      BrowserPopupUtils.setContentScrollY(window, this.state?.scrollY);
     }
 
     // Load all sends if sync completed in background
@@ -172,7 +171,7 @@ export class SendGroupingsComponent extends BaseSendComponent {
 
   private async saveState() {
     this.state = Object.assign(new BrowserSendComponentState(), {
-      scrollY: this.popupUtils.getContentScrollY(window),
+      scrollY: BrowserPopupUtils.getContentScrollY(window),
       searchText: this.searchText,
       sends: this.sends,
       typeCounts: this.typeCounts,
diff --git a/apps/browser/src/tools/popup/send/send-type.component.ts b/apps/browser/src/tools/popup/send/send-type.component.ts
index 4a2794fdda5..6e5e76a0e5d 100644
--- a/apps/browser/src/tools/popup/send/send-type.component.ts
+++ b/apps/browser/src/tools/popup/send/send-type.component.ts
@@ -18,8 +18,8 @@ import { SendService } from "@bitwarden/common/tools/send/services/send.service.
 import { DialogService } from "@bitwarden/components";
 
 import { BrowserComponentState } from "../../../models/browserComponentState";
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
 import { BrowserStateService } from "../../../platform/services/abstractions/browser-state.service";
-import { PopupUtilsService } from "../../../popup/services/popup-utils.service";
 
 const ComponentId = "SendTypeComponent";
 
@@ -42,7 +42,6 @@ export class SendTypeComponent extends BaseSendComponent {
     ngZone: NgZone,
     policyService: PolicyService,
     searchService: SearchService,
-    private popupUtils: PopupUtilsService,
     private stateService: BrowserStateService,
     private route: ActivatedRoute,
     private location: Location,
@@ -102,7 +101,7 @@ export class SendTypeComponent extends BaseSendComponent {
 
       // Restore state and remove reference
       if (this.applySavedState && this.state != null) {
-        window.setTimeout(() => this.popupUtils.setContentScrollY(window, this.state?.scrollY), 0);
+        BrowserPopupUtils.setContentScrollY(window, this.state?.scrollY);
       }
       this.stateService.setBrowserSendTypeComponentState(null);
     });
@@ -163,7 +162,7 @@ export class SendTypeComponent extends BaseSendComponent {
 
   private async saveState() {
     this.state = {
-      scrollY: this.popupUtils.getContentScrollY(window),
+      scrollY: BrowserPopupUtils.getContentScrollY(window),
       searchText: this.searchText,
     };
     await this.stateService.setBrowserSendTypeComponentState(this.state);
diff --git a/apps/browser/src/tools/popup/services/file-popout-utils.service.ts b/apps/browser/src/tools/popup/services/file-popout-utils.service.ts
index 0dde2b1a3d2..65a311e47c3 100644
--- a/apps/browser/src/tools/popup/services/file-popout-utils.service.ts
+++ b/apps/browser/src/tools/popup/services/file-popout-utils.service.ts
@@ -2,7 +2,7 @@ import { Injectable } from "@angular/core";
 
 import { PlatformUtilsService } from "@bitwarden/common/platform/abstractions/platform-utils.service";
 
-import { PopupUtilsService } from "../../../popup/services/popup-utils.service";
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
 
 /**
  * Service for determining whether to display file popout callout messages.
@@ -12,10 +12,7 @@ export class FilePopoutUtilsService {
   /**
    * Creates an instance of FilePopoutUtilsService.
    */
-  constructor(
-    private platformUtilsService: PlatformUtilsService,
-    private popupUtilsService: PopupUtilsService
-  ) {}
+  constructor(private platformUtilsService: PlatformUtilsService) {}
 
   /**
    * Determines whether to show any file popout callout message in the current browser.
@@ -38,7 +35,7 @@ export class FilePopoutUtilsService {
   showFirefoxFileWarning(win: Window): boolean {
     return (
       this.platformUtilsService.isFirefox() &&
-      !(this.popupUtilsService.inSidebar(win) || this.popupUtilsService.inPopout(win))
+      !(BrowserPopupUtils.inSidebar(win) || BrowserPopupUtils.inPopout(win))
     );
   }
 
@@ -48,7 +45,7 @@ export class FilePopoutUtilsService {
    * @returns True if the extension is not in a popout; otherwise, false.
    */
   showSafariFileWarning(win: Window): boolean {
-    return this.platformUtilsService.isSafari() && !this.popupUtilsService.inPopout(win);
+    return this.platformUtilsService.isSafari() && !BrowserPopupUtils.inPopout(win);
   }
 
   /**
@@ -60,7 +57,7 @@ export class FilePopoutUtilsService {
     return (
       (this.isLinux(win) || this.isUnsupportedMac(win)) &&
       !this.platformUtilsService.isFirefox() &&
-      !(this.popupUtilsService.inSidebar(win) || this.popupUtilsService.inPopout(win))
+      !(BrowserPopupUtils.inSidebar(win) || BrowserPopupUtils.inPopout(win))
     );
   }
 
diff --git a/apps/browser/src/vault/fido2/browser-fido2-user-interface.service.ts b/apps/browser/src/vault/fido2/browser-fido2-user-interface.service.ts
index 5eab5849c41..71aae01c549 100644
--- a/apps/browser/src/vault/fido2/browser-fido2-user-interface.service.ts
+++ b/apps/browser/src/vault/fido2/browser-fido2-user-interface.service.ts
@@ -29,7 +29,7 @@ import {
 } from "@bitwarden/common/vault/abstractions/fido2/fido2-user-interface.service.abstraction";
 
 import { BrowserApi } from "../../platform/browser/browser-api";
-import { BrowserPopoutWindowService } from "../../platform/popup/abstractions/browser-popout-window.service";
+import { closeFido2Popout, openFido2Popout } from "../popup/utils/vault-popout-window";
 
 const BrowserFido2MessageName = "BrowserFido2UserInterfaceServiceMessage";
 
@@ -116,10 +116,7 @@ export type BrowserFido2Message = { sessionId: string } & (
  * The user interface is implemented as a popout and the service uses the browser's messaging API to communicate with it.
  */
 export class BrowserFido2UserInterfaceService implements Fido2UserInterfaceServiceAbstraction {
-  constructor(
-    private browserPopoutWindowService: BrowserPopoutWindowService,
-    private authService: AuthService
-  ) {}
+  constructor(private authService: AuthService) {}
 
   async newSession(
     fallbackSupported: boolean,
@@ -127,7 +124,6 @@ export class BrowserFido2UserInterfaceService implements Fido2UserInterfaceServi
     abortController?: AbortController
   ): Promise<Fido2UserInterfaceSession> {
     return await BrowserFido2UserInterfaceSession.create(
-      this.browserPopoutWindowService,
       this.authService,
       fallbackSupported,
       tab,
@@ -138,14 +134,12 @@ export class BrowserFido2UserInterfaceService implements Fido2UserInterfaceServi
 
 export class BrowserFido2UserInterfaceSession implements Fido2UserInterfaceSession {
   static async create(
-    browserPopoutWindowService: BrowserPopoutWindowService,
     authService: AuthService,
     fallbackSupported: boolean,
     tab: chrome.tabs.Tab,
     abortController?: AbortController
   ): Promise<BrowserFido2UserInterfaceSession> {
     return new BrowserFido2UserInterfaceSession(
-      browserPopoutWindowService,
       authService,
       fallbackSupported,
       tab,
@@ -183,7 +177,6 @@ export class BrowserFido2UserInterfaceSession implements Fido2UserInterfaceSessi
   private destroy$ = new Subject<void>();
 
   private constructor(
-    private readonly browserPopoutWindowService: BrowserPopoutWindowService,
     private readonly authService: AuthService,
     private readonly fallbackSupported: boolean,
     private readonly tab: chrome.tabs.Tab,
@@ -304,7 +297,7 @@ export class BrowserFido2UserInterfaceSession implements Fido2UserInterfaceSessi
   }
 
   async close() {
-    await this.browserPopoutWindowService.closeFido2Popout();
+    await closeFido2Popout(this.sessionId);
     this.closed = true;
     this.destroy$.next();
     this.destroy$.complete();
@@ -354,9 +347,8 @@ export class BrowserFido2UserInterfaceSession implements Fido2UserInterfaceSessi
       )
     );
 
-    const popoutId = await this.browserPopoutWindowService.openFido2Popout(this.tab, {
+    const popoutId = await openFido2Popout(this.tab, {
       sessionId: this.sessionId,
-      senderTabId: this.tab.id,
       fallbackSupported: this.fallbackSupported,
     });
 
diff --git a/apps/browser/src/vault/popup/components/fido2/fido2.component.ts b/apps/browser/src/vault/popup/components/fido2/fido2.component.ts
index 6f0bf96deec..c0862ab5081 100644
--- a/apps/browser/src/vault/popup/components/fido2/fido2.component.ts
+++ b/apps/browser/src/vault/popup/components/fido2/fido2.component.ts
@@ -35,6 +35,7 @@ import {
   BrowserFido2Message,
   BrowserFido2UserInterfaceSession,
 } from "../../../fido2/browser-fido2-user-interface.service";
+import { VaultPopoutType } from "../../utils/vault-popout-window";
 
 interface ViewData {
   message: BrowserFido2Message;
@@ -280,6 +281,7 @@ export class Fido2Component implements OnInit, OnDestroy {
         uilocation: "popout",
         senderTabId: this.senderTabId,
         sessionId: this.sessionId,
+        singleActionPopout: `${VaultPopoutType.fido2Popout}_${this.sessionId}`,
       },
     });
   }
@@ -299,6 +301,7 @@ export class Fido2Component implements OnInit, OnDestroy {
         senderTabId: this.senderTabId,
         sessionId: this.sessionId,
         userVerification: data.userVerification,
+        singleActionPopout: `${VaultPopoutType.fido2Popout}_${this.sessionId}`,
       },
     });
   }
diff --git a/apps/browser/src/vault/popup/components/vault/add-edit.component.ts b/apps/browser/src/vault/popup/components/vault/add-edit.component.ts
index 9b832148a86..9dbf619676a 100644
--- a/apps/browser/src/vault/popup/components/vault/add-edit.component.ts
+++ b/apps/browser/src/vault/popup/components/vault/add-edit.component.ts
@@ -24,11 +24,13 @@ import { DialogService } from "@bitwarden/components";
 import { PasswordRepromptService } from "@bitwarden/vault";
 
 import { BrowserApi } from "../../../../platform/browser/browser-api";
-import { PopupUtilsService } from "../../../../popup/services/popup-utils.service";
+import BrowserPopupUtils from "../../../../platform/popup/browser-popup-utils";
+import { PopupCloseWarningService } from "../../../../popup/services/popup-close-warning.service";
 import {
   BrowserFido2UserInterfaceSession,
   fido2PopoutSessionData$,
 } from "../../../fido2/browser-fido2-user-interface.service";
+import { VaultPopoutType, closeAddEditVaultItemPopout } from "../../utils/vault-popout-window";
 
 @Component({
   selector: "app-vault-add-edit",
@@ -40,9 +42,7 @@ export class AddEditComponent extends BaseAddEditComponent {
   showAttachments = true;
   openAttachmentsInPopup: boolean;
   showAutoFillOnPageLoadOptions: boolean;
-  senderTabId?: number;
-  uilocation?: "popout" | "popup" | "sidebar" | "tab";
-  inPopout = false;
+  private singleActionKey: string;
 
   private fido2PopoutSessionData$ = fido2PopoutSessionData$();
 
@@ -60,7 +60,7 @@ export class AddEditComponent extends BaseAddEditComponent {
     private location: Location,
     eventCollectionService: EventCollectionService,
     policyService: PolicyService,
-    private popupUtilsService: PopupUtilsService,
+    private popupCloseWarningService: PopupCloseWarningService,
     organizationService: OrganizationService,
     passwordRepromptService: PasswordRepromptService,
     logService: LogService,
@@ -91,9 +91,6 @@ export class AddEditComponent extends BaseAddEditComponent {
 
     // eslint-disable-next-line rxjs-angular/prefer-takeuntil, rxjs/no-async-subscribe
     this.route.queryParams.pipe(first()).subscribe(async (params) => {
-      this.senderTabId = parseInt(params?.senderTabId, 10) || undefined;
-      this.uilocation = params?.uilocation;
-
       if (params.cipherId) {
         this.cipherId = params.cipherId;
       }
@@ -119,18 +116,16 @@ export class AddEditComponent extends BaseAddEditComponent {
       if (params.selectedVault) {
         this.organizationId = params.selectedVault;
       }
+      if (params.singleActionKey) {
+        this.singleActionKey = params.singleActionKey;
+      }
       await this.load();
 
       if (!this.editMode || this.cloneMode) {
-        if (
-          !this.popupUtilsService.inPopout(window) &&
-          params.name &&
-          (this.cipher.name == null || this.cipher.name === "")
-        ) {
+        if (params.name && (this.cipher.name == null || this.cipher.name === "")) {
           this.cipher.name = params.name;
         }
         if (
-          !this.popupUtilsService.inPopout(window) &&
           params.uri &&
           (this.cipher.login.uris[0].uri == null || this.cipher.login.uris[0].uri === "")
         ) {
@@ -138,11 +133,9 @@ export class AddEditComponent extends BaseAddEditComponent {
         }
       }
 
-      this.openAttachmentsInPopup = this.popupUtilsService.inPopup(window);
+      this.openAttachmentsInPopup = BrowserPopupUtils.inPopup(window);
     });
 
-    this.inPopout = this.uilocation === "popout" || this.popupUtilsService.inPopout(window);
-
     if (!this.editMode) {
       const tabs = await BrowserApi.tabsQuery({ windowType: "normal" });
       this.currentUris =
@@ -153,8 +146,8 @@ export class AddEditComponent extends BaseAddEditComponent {
 
     this.setFocus();
 
-    if (this.popupUtilsService.inTab(window)) {
-      this.popupUtilsService.enableCloseTabWarning();
+    if (BrowserPopupUtils.inPopout(window)) {
+      this.popupCloseWarningService.enable();
     }
   }
 
@@ -167,12 +160,10 @@ export class AddEditComponent extends BaseAddEditComponent {
 
   async submit(): Promise<boolean> {
     const fido2SessionData = await firstValueFrom(this.fido2PopoutSessionData$);
-    // Would be refactored after rework is done on the windows popout service
-
     const { isFido2Session, sessionId, userVerification } = fido2SessionData;
+    const inFido2PopoutWindow = BrowserPopupUtils.inPopout(window) && isFido2Session;
     if (
-      this.inPopout &&
-      isFido2Session &&
+      inFido2PopoutWindow &&
       !(await this.handleFido2UserVerification(sessionId, userVerification))
     ) {
       return false;
@@ -183,7 +174,11 @@ export class AddEditComponent extends BaseAddEditComponent {
       return false;
     }
 
-    if (this.inPopout && isFido2Session) {
+    if (BrowserPopupUtils.inPopout(window)) {
+      this.popupCloseWarningService.disable();
+    }
+
+    if (inFido2PopoutWindow) {
       BrowserFido2UserInterfaceSession.confirmNewCredentialResponse(
         sessionId,
         this.cipher.id,
@@ -192,14 +187,8 @@ export class AddEditComponent extends BaseAddEditComponent {
       return true;
     }
 
-    if (this.popupUtilsService.inTab(window)) {
-      this.popupUtilsService.disableCloseTabWarning();
-      this.messagingService.send("closeTab", { delay: 1000 });
-      return true;
-    }
-
-    if (this.senderTabId && this.inPopout) {
-      setTimeout(() => this.close(), 1000);
+    if (this.inAddEditPopoutWindow()) {
+      await closeAddEditVaultItemPopout(1000);
       return true;
     }
 
@@ -219,7 +208,7 @@ export class AddEditComponent extends BaseAddEditComponent {
         .createUrlTree(["/attachments"], { queryParams: { cipherId: this.cipher.id } })
         .toString();
       const currentBaseUrl = window.location.href.replace(this.router.url, "");
-      this.popupUtilsService.popOut(window, currentBaseUrl + destinationUrl);
+      BrowserPopupUtils.openCurrentPagePopout(window, currentBaseUrl + destinationUrl);
     } else {
       this.router.navigate(["/attachments"], { queryParams: { cipherId: this.cipher.id } });
     }
@@ -235,34 +224,21 @@ export class AddEditComponent extends BaseAddEditComponent {
   async cancel() {
     super.cancel();
 
-    // Would be refactored after rework is done on the windows popout service
     const sessionData = await firstValueFrom(this.fido2PopoutSessionData$);
-    if (this.inPopout && sessionData.isFido2Session) {
+    if (BrowserPopupUtils.inPopout(window) && sessionData.isFido2Session) {
+      this.popupCloseWarningService.disable();
       BrowserFido2UserInterfaceSession.abortPopout(sessionData.sessionId);
       return;
     }
 
-    if (this.senderTabId && this.inPopout) {
-      this.close();
-      return;
-    }
-
-    if (this.popupUtilsService.inTab(window)) {
-      this.messagingService.send("closeTab");
+    if (this.inAddEditPopoutWindow()) {
+      closeAddEditVaultItemPopout();
       return;
     }
 
     this.location.back();
   }
 
-  // Used for closing single-action views
-  close() {
-    BrowserApi.focusTab(this.senderTabId);
-    window.close();
-
-    return;
-  }
-
   async generateUsername(): Promise<boolean> {
     const confirmed = await super.generateUsername();
     if (confirmed) {
@@ -356,4 +332,11 @@ export class AddEditComponent extends BaseAddEditComponent {
       this.i18nService.t("autofillOnPageLoadSetToDefault")
     );
   }
+
+  private inAddEditPopoutWindow() {
+    return BrowserPopupUtils.inSingleActionPopout(
+      window,
+      this.singleActionKey || VaultPopoutType.addEditVaultItem
+    );
+  }
 }
diff --git a/apps/browser/src/vault/popup/components/vault/current-tab.component.ts b/apps/browser/src/vault/popup/components/vault/current-tab.component.ts
index 4f1ceb466de..a7a40131a12 100644
--- a/apps/browser/src/vault/popup/components/vault/current-tab.component.ts
+++ b/apps/browser/src/vault/popup/components/vault/current-tab.component.ts
@@ -19,7 +19,7 @@ import { PasswordRepromptService } from "@bitwarden/vault";
 
 import { AutofillService } from "../../../../autofill/services/abstractions/autofill.service";
 import { BrowserApi } from "../../../../platform/browser/browser-api";
-import { PopupUtilsService } from "../../../../popup/services/popup-utils.service";
+import BrowserPopupUtils from "../../../../platform/popup/browser-popup-utils";
 import { VaultFilterService } from "../../../services/vault-filter.service";
 
 const BroadcasterSubscriptionId = "CurrentTabComponent";
@@ -55,7 +55,6 @@ export class CurrentTabComponent implements OnInit, OnDestroy {
   constructor(
     private platformUtilsService: PlatformUtilsService,
     private cipherService: CipherService,
-    private popupUtilsService: PopupUtilsService,
     private autofillService: AutofillService,
     private i18nService: I18nService,
     private router: Router,
@@ -72,7 +71,7 @@ export class CurrentTabComponent implements OnInit, OnDestroy {
 
   async ngOnInit() {
     this.searchTypeSearch = !this.platformUtilsService.isSafari();
-    this.inSidebar = this.popupUtilsService.inSidebar(window);
+    this.inSidebar = BrowserPopupUtils.inSidebar(window);
 
     this.broadcasterService.subscribe(BroadcasterSubscriptionId, (message: any) => {
       this.ngZone.run(async () => {
@@ -185,7 +184,7 @@ export class CurrentTabComponent implements OnInit, OnDestroy {
       if (this.totpCode != null) {
         this.platformUtilsService.copyToClipboard(this.totpCode, { window: window });
       }
-      if (this.popupUtilsService.inPopup(window)) {
+      if (BrowserPopupUtils.inPopup(window)) {
         if (!closePopupDelay) {
           if (this.platformUtilsService.isFirefox() || this.platformUtilsService.isSafari()) {
             BrowserApi.closePopup(window);
diff --git a/apps/browser/src/vault/popup/components/vault/vault-filter.component.ts b/apps/browser/src/vault/popup/components/vault/vault-filter.component.ts
index 4be0fe89fe1..f6d0ae96fd7 100644
--- a/apps/browser/src/vault/popup/components/vault/vault-filter.component.ts
+++ b/apps/browser/src/vault/popup/components/vault/vault-filter.component.ts
@@ -19,8 +19,8 @@ import { FolderView } from "@bitwarden/common/vault/models/view/folder.view";
 
 import { BrowserGroupingsComponentState } from "../../../../models/browserGroupingsComponentState";
 import { BrowserApi } from "../../../../platform/browser/browser-api";
+import BrowserPopupUtils from "../../../../platform/popup/browser-popup-utils";
 import { BrowserStateService } from "../../../../platform/services/abstractions/browser-state.service";
-import { PopupUtilsService } from "../../../../popup/services/popup-utils.service";
 import { VaultFilterService } from "../../../services/vault-filter.service";
 
 const ComponentId = "VaultComponent";
@@ -80,7 +80,6 @@ export class VaultFilterComponent implements OnInit, OnDestroy {
     private broadcasterService: BroadcasterService,
     private changeDetectorRef: ChangeDetectorRef,
     private route: ActivatedRoute,
-    private popupUtils: PopupUtilsService,
     private syncService: SyncService,
     private platformUtilsService: PlatformUtilsService,
     private searchService: SearchService,
@@ -94,7 +93,7 @@ export class VaultFilterComponent implements OnInit, OnDestroy {
   async ngOnInit() {
     this.searchTypeSearch = !this.platformUtilsService.isSafari();
     this.showLeftHeader = !(
-      this.popupUtils.inSidebar(window) && this.platformUtilsService.isFirefox()
+      BrowserPopupUtils.inSidebar(window) && this.platformUtilsService.isFirefox()
     );
     await this.browserStateService.setBrowserVaultItemsComponentState(null);
 
@@ -136,7 +135,7 @@ export class VaultFilterComponent implements OnInit, OnDestroy {
       }
 
       if (!this.syncService.syncInProgress || restoredScopeState) {
-        window.setTimeout(() => this.popupUtils.setContentScrollY(window, this.state?.scrollY), 0);
+        BrowserPopupUtils.setContentScrollY(window, this.state?.scrollY);
       }
     });
   }
@@ -265,7 +264,7 @@ export class VaultFilterComponent implements OnInit, OnDestroy {
     this.preventSelected = true;
     await this.cipherService.updateLastLaunchedDate(cipher.id);
     BrowserApi.createNewTab(cipher.login.launchUri);
-    if (this.popupUtils.inPopup(window)) {
+    if (BrowserPopupUtils.inPopup(window)) {
       BrowserApi.closePopup(window);
     }
   }
@@ -376,7 +375,7 @@ export class VaultFilterComponent implements OnInit, OnDestroy {
 
   private async saveState() {
     this.state = Object.assign(new BrowserGroupingsComponentState(), {
-      scrollY: this.popupUtils.getContentScrollY(window),
+      scrollY: BrowserPopupUtils.getContentScrollY(window),
       searchText: this.searchText,
       favoriteCiphers: this.favoriteCiphers,
       noFolderCiphers: this.noFolderCiphers,
diff --git a/apps/browser/src/vault/popup/components/vault/vault-items.component.ts b/apps/browser/src/vault/popup/components/vault/vault-items.component.ts
index 59d7ae92c28..32e7a9eacda 100644
--- a/apps/browser/src/vault/popup/components/vault/vault-items.component.ts
+++ b/apps/browser/src/vault/popup/components/vault/vault-items.component.ts
@@ -13,7 +13,6 @@ import { I18nService } from "@bitwarden/common/platform/abstractions/i18n.servic
 import { PlatformUtilsService } from "@bitwarden/common/platform/abstractions/platform-utils.service";
 import { CipherService } from "@bitwarden/common/vault/abstractions/cipher.service";
 import { CollectionService } from "@bitwarden/common/vault/abstractions/collection.service";
-import { FolderService } from "@bitwarden/common/vault/abstractions/folder/folder.service.abstraction";
 import { CipherType } from "@bitwarden/common/vault/enums/cipher-type";
 import { CipherView } from "@bitwarden/common/vault/models/view/cipher.view";
 import { CollectionView } from "@bitwarden/common/vault/models/view/collection.view";
@@ -21,8 +20,8 @@ import { FolderView } from "@bitwarden/common/vault/models/view/folder.view";
 
 import { BrowserComponentState } from "../../../../models/browserComponentState";
 import { BrowserApi } from "../../../../platform/browser/browser-api";
+import BrowserPopupUtils from "../../../../platform/popup/browser-popup-utils";
 import { BrowserStateService } from "../../../../platform/services/abstractions/browser-state.service";
-import { PopupUtilsService } from "../../../../popup/services/popup-utils.service";
 import { VaultFilterService } from "../../../services/vault-filter.service";
 
 const ComponentId = "VaultItemsComponent";
@@ -61,9 +60,7 @@ export class VaultItemsComponent extends BaseVaultItemsComponent implements OnIn
     private broadcasterService: BroadcasterService,
     private changeDetectorRef: ChangeDetectorRef,
     private stateService: BrowserStateService,
-    private popupUtils: PopupUtilsService,
     private i18nService: I18nService,
-    private folderService: FolderService,
     private collectionService: CollectionService,
     private platformUtilsService: PlatformUtilsService,
     cipherService: CipherService,
@@ -155,11 +152,10 @@ export class VaultItemsComponent extends BaseVaultItemsComponent implements OnIn
       }
 
       if (this.applySavedState && this.state != null) {
-        window.setTimeout(
-          () =>
-            this.popupUtils.setContentScrollY(window, this.state.scrollY, this.scrollingContainer),
-          0
-        );
+        BrowserPopupUtils.setContentScrollY(window, this.state.scrollY, {
+          delay: 0,
+          containerSelector: this.scrollingContainer,
+        });
       }
       await this.stateService.setBrowserVaultItemsComponentState(null);
     });
@@ -219,7 +215,7 @@ export class VaultItemsComponent extends BaseVaultItemsComponent implements OnIn
     this.preventSelected = true;
     await this.cipherService.updateLastLaunchedDate(cipher.id);
     BrowserApi.createNewTab(cipher.login.launchUri);
-    if (this.popupUtils.inPopup(window)) {
+    if (BrowserPopupUtils.inPopup(window)) {
       BrowserApi.closePopup(window);
     }
   }
@@ -288,7 +284,7 @@ export class VaultItemsComponent extends BaseVaultItemsComponent implements OnIn
 
   private async saveState() {
     this.state = {
-      scrollY: this.popupUtils.getContentScrollY(window, this.scrollingContainer),
+      scrollY: BrowserPopupUtils.getContentScrollY(window, this.scrollingContainer),
       searchText: this.searchText,
     };
     await this.stateService.setBrowserVaultItemsComponentState(this.state);
diff --git a/apps/browser/src/vault/popup/components/vault/view.component.ts b/apps/browser/src/vault/popup/components/vault/view.component.ts
index b29814ed559..6e7adb62103 100644
--- a/apps/browser/src/vault/popup/components/vault/view.component.ts
+++ b/apps/browser/src/vault/popup/components/vault/view.component.ts
@@ -28,7 +28,7 @@ import { PasswordRepromptService } from "@bitwarden/vault";
 
 import { AutofillService } from "../../../../autofill/services/abstractions/autofill.service";
 import { BrowserApi } from "../../../../platform/browser/browser-api";
-import { PopupUtilsService } from "../../../../popup/services/popup-utils.service";
+import BrowserPopupUtils from "../../../../platform/popup/browser-popup-utils";
 import {
   BrowserFido2UserInterfaceSession,
   fido2PopoutSessionData$,
@@ -84,7 +84,6 @@ export class ViewComponent extends BaseViewComponent {
     eventCollectionService: EventCollectionService,
     private autofillService: AutofillService,
     private messagingService: MessagingService,
-    private popupUtilsService: PopupUtilsService,
     apiService: ApiService,
     passwordRepromptService: PasswordRepromptService,
     logService: LogService,
@@ -121,7 +120,7 @@ export class ViewComponent extends BaseViewComponent {
       this.uilocation = value?.uilocation;
     });
 
-    this.inPopout = this.uilocation === "popout" || this.popupUtilsService.inPopout(window);
+    this.inPopout = this.uilocation === "popout" || BrowserPopupUtils.inPopout(window);
 
     // eslint-disable-next-line rxjs-angular/prefer-takeuntil, rxjs/no-async-subscribe
     this.route.queryParams.pipe(first()).subscribe(async (params) => {
diff --git a/apps/browser/src/vault/popup/utils/vault-popout-window.spec.ts b/apps/browser/src/vault/popup/utils/vault-popout-window.spec.ts
new file mode 100644
index 00000000000..06fb25665b3
--- /dev/null
+++ b/apps/browser/src/vault/popup/utils/vault-popout-window.spec.ts
@@ -0,0 +1,149 @@
+import { mock } from "jest-mock-extended";
+
+import { CipherType } from "@bitwarden/common/vault/enums/cipher-type";
+
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
+
+import {
+  closeAddEditVaultItemPopout,
+  closeFido2Popout,
+  openAddEditVaultItemPopout,
+  openFido2Popout,
+  openVaultItemPasswordRepromptPopout,
+  VaultPopoutType,
+} from "./vault-popout-window";
+
+describe("VaultPopoutWindow", () => {
+  const openPopoutSpy = jest
+    .spyOn(BrowserPopupUtils, "openPopout")
+    .mockResolvedValue(mock<chrome.windows.Window>({ id: 10 }));
+  const closeSingleActionPopoutSpy = jest
+    .spyOn(BrowserPopupUtils, "closeSingleActionPopout")
+    .mockImplementation();
+
+  afterEach(() => {
+    jest.clearAllMocks();
+  });
+
+  describe("openVaultItemPasswordRepromptPopout", () => {
+    it("opens a popout window that facilitates re-prompting for the password of a vault item", async () => {
+      const senderTab = { windowId: 1 } as chrome.tabs.Tab;
+
+      await openVaultItemPasswordRepromptPopout(senderTab, {
+        cipherId: "cipherId",
+        action: "action",
+      });
+
+      expect(openPopoutSpy).toHaveBeenCalledWith(
+        "popup/index.html#/view-cipher?cipherId=cipherId&senderTabId=undefined&action=action",
+        {
+          singleActionKey: `${VaultPopoutType.vaultItemPasswordReprompt}_cipherId`,
+          senderWindowId: 1,
+          forceCloseExistingWindows: true,
+        }
+      );
+    });
+  });
+
+  describe("openAddEditVaultItemPopout", () => {
+    it("opens a popout window that facilitates adding a vault item", async () => {
+      await openAddEditVaultItemPopout(
+        mock<chrome.tabs.Tab>({ windowId: 1, url: "https://tacos.com" })
+      );
+
+      expect(openPopoutSpy).toHaveBeenCalledWith(
+        "popup/index.html#/edit-cipher?uilocation=popout&uri=https://tacos.com",
+        {
+          singleActionKey: VaultPopoutType.addEditVaultItem,
+          senderWindowId: 1,
+        }
+      );
+    });
+
+    it("opens a popout window that facilitates adding a specific type of vault item", () => {
+      openAddEditVaultItemPopout(mock<chrome.tabs.Tab>({ windowId: 1, url: "https://tacos.com" }), {
+        cipherType: CipherType.Identity,
+      });
+
+      expect(openPopoutSpy).toHaveBeenCalledWith(
+        `popup/index.html#/edit-cipher?uilocation=popout&type=${CipherType.Identity}&uri=https://tacos.com`,
+        {
+          singleActionKey: `${VaultPopoutType.addEditVaultItem}_${CipherType.Identity}`,
+          senderWindowId: 1,
+        }
+      );
+    });
+
+    it("opens a popout window that facilitates editing a vault item", async () => {
+      await openAddEditVaultItemPopout(
+        mock<chrome.tabs.Tab>({ windowId: 1, url: "https://tacos.com" }),
+        {
+          cipherId: "cipherId",
+        }
+      );
+
+      expect(openPopoutSpy).toHaveBeenCalledWith(
+        "popup/index.html#/edit-cipher?uilocation=popout&cipherId=cipherId&uri=https://tacos.com",
+        {
+          singleActionKey: `${VaultPopoutType.addEditVaultItem}_cipherId`,
+          senderWindowId: 1,
+        }
+      );
+    });
+  });
+
+  describe("closeAddEditVaultItemPopout", () => {
+    it("closes the add/edit vault item popout window", () => {
+      closeAddEditVaultItemPopout();
+
+      expect(closeSingleActionPopoutSpy).toHaveBeenCalledWith(VaultPopoutType.addEditVaultItem, 0);
+    });
+
+    it("closes the add/edit vault item popout window after a delay", () => {
+      closeAddEditVaultItemPopout(1000);
+
+      expect(closeSingleActionPopoutSpy).toHaveBeenCalledWith(
+        VaultPopoutType.addEditVaultItem,
+        1000
+      );
+    });
+  });
+
+  describe("openFido2Popout", () => {
+    it("opens a popout window that facilitates FIDO2 authentication workflows", async () => {
+      const senderTab = mock<chrome.tabs.Tab>({
+        windowId: 1,
+        url: "https://jest-testing.com",
+        id: 2,
+      });
+
+      const returnedWindowId = await openFido2Popout(senderTab, {
+        sessionId: "sessionId",
+        fallbackSupported: true,
+      });
+
+      expect(openPopoutSpy).toHaveBeenCalledWith(
+        "popup/index.html#/fido2?sessionId=sessionId&fallbackSupported=true&senderTabId=2&senderUrl=https%3A%2F%2Fjest-testing.com",
+        {
+          singleActionKey: `${VaultPopoutType.fido2Popout}_sessionId`,
+          senderWindowId: 1,
+          forceCloseExistingWindows: true,
+          windowOptions: { height: 450 },
+        }
+      );
+      expect(returnedWindowId).toEqual(10);
+    });
+  });
+
+  describe("closeFido2Popout", () => {
+    it("closes the fido2 popout window", () => {
+      const sessionId = "sessionId";
+
+      closeFido2Popout(sessionId);
+
+      expect(closeSingleActionPopoutSpy).toHaveBeenCalledWith(
+        `${VaultPopoutType.fido2Popout}_${sessionId}`
+      );
+    });
+  });
+});
diff --git a/apps/browser/src/vault/popup/utils/vault-popout-window.ts b/apps/browser/src/vault/popup/utils/vault-popout-window.ts
new file mode 100644
index 00000000000..3989aa076ac
--- /dev/null
+++ b/apps/browser/src/vault/popup/utils/vault-popout-window.ts
@@ -0,0 +1,129 @@
+import { CipherType } from "@bitwarden/common/vault/enums/cipher-type";
+
+import BrowserPopupUtils from "../../../platform/popup/browser-popup-utils";
+
+const VaultPopoutType = {
+  vaultItemPasswordReprompt: "vault_PasswordReprompt",
+  addEditVaultItem: "vault_AddEditVaultItem",
+  fido2Popout: "vault_Fido2Popout",
+} as const;
+
+/**
+ * Opens a popout window that facilitates re-prompting for
+ * the password of a vault item.
+ *
+ * @param senderTab - The tab that sent the request.
+ * @param cipherOptions - The cipher id and action to perform.
+ */
+async function openVaultItemPasswordRepromptPopout(
+  senderTab: chrome.tabs.Tab,
+  cipherOptions: {
+    cipherId: string;
+    action: string;
+  }
+) {
+  const { cipherId, action } = cipherOptions;
+  const promptWindowPath =
+    "popup/index.html#/view-cipher" +
+    `?cipherId=${cipherId}` +
+    `&senderTabId=${senderTab.id}` +
+    `&action=${action}`;
+
+  await BrowserPopupUtils.openPopout(promptWindowPath, {
+    singleActionKey: `${VaultPopoutType.vaultItemPasswordReprompt}_${cipherId}`,
+    senderWindowId: senderTab.windowId,
+    forceCloseExistingWindows: true,
+  });
+}
+
+/**
+ * Opens a popout window that facilitates adding or editing a vault item.
+ *
+ * @param senderTab - The window id of the sender.
+ * @param cipherOptions - Options passed as query params to the popout.
+ */
+async function openAddEditVaultItemPopout(
+  senderTab: chrome.tabs.Tab,
+  cipherOptions: { cipherId?: string; cipherType?: CipherType } = {}
+) {
+  const { cipherId, cipherType } = cipherOptions;
+  const { url, windowId } = senderTab;
+
+  let singleActionKey = VaultPopoutType.addEditVaultItem;
+  let addEditCipherUrl = "popup/index.html#/edit-cipher?uilocation=popout";
+  if (cipherId && !cipherType) {
+    singleActionKey += `_${cipherId}`;
+    addEditCipherUrl += `&cipherId=${cipherId}`;
+  }
+  if (cipherType && !cipherId) {
+    singleActionKey += `_${cipherType}`;
+    addEditCipherUrl += `&type=${cipherType}`;
+  }
+  if (senderTab.url) {
+    addEditCipherUrl += `&uri=${url}`;
+  }
+
+  await BrowserPopupUtils.openPopout(addEditCipherUrl, {
+    singleActionKey,
+    senderWindowId: windowId,
+  });
+}
+
+/**
+ * Closes the add/edit vault item popout window.
+ *
+ * @param delayClose - The amount of time to wait before closing the popout. Defaults to 0.
+ */
+async function closeAddEditVaultItemPopout(delayClose = 0) {
+  await BrowserPopupUtils.closeSingleActionPopout(VaultPopoutType.addEditVaultItem, delayClose);
+}
+
+/**
+ * Opens a popout window that facilitates FIDO2
+ * authentication and passkey management.
+ *
+ * @param senderTab - The tab that sent the request.
+ * @param options - Options passed as query params to the popout.
+ */
+async function openFido2Popout(
+  senderTab: chrome.tabs.Tab,
+  options: {
+    sessionId: string;
+    fallbackSupported: boolean;
+  }
+): Promise<chrome.windows.Window["id"]> {
+  const { sessionId, fallbackSupported } = options;
+  const promptWindowPath =
+    "popup/index.html#/fido2" +
+    `?sessionId=${sessionId}` +
+    `&fallbackSupported=${fallbackSupported}` +
+    `&senderTabId=${senderTab.id}` +
+    `&senderUrl=${encodeURIComponent(senderTab.url)}`;
+
+  const popoutWindow = await BrowserPopupUtils.openPopout(promptWindowPath, {
+    singleActionKey: `${VaultPopoutType.fido2Popout}_${sessionId}`,
+    senderWindowId: senderTab.windowId,
+    forceCloseExistingWindows: true,
+    windowOptions: { height: 450 },
+  });
+
+  return popoutWindow.id;
+}
+
+/**
+ * Closes the FIDO2 popout window associated with the passed session ID.
+ *
+ * @param sessionId - The session ID of the popout to close.
+ */
+async function closeFido2Popout(sessionId: string): Promise<void> {
+  await BrowserPopupUtils.closeSingleActionPopout(`${VaultPopoutType.fido2Popout}_${sessionId}`);
+}
+
+export {
+  VaultPopoutType,
+  openVaultItemPasswordRepromptPopout,
+  openAddEditVaultItemPopout,
+  closeAddEditVaultItemPopout,
+  openFido2Popout,
+  closeFido2Popout,
+};
diff --git a/apps/browser/test.setup.ts b/apps/browser/test.setup.ts
index 6feb163e0a6..b6d2fce9db8 100644
--- a/apps/browser/test.setup.ts
+++ b/apps/browser/test.setup.ts
@@ -23,6 +23,7 @@ const runtime = {
   },
   sendMessage: jest.fn(),
   getManifest: jest.fn(),
+  getURL: jest.fn((path) => `chrome-extension://id/${path}`),
 };
 
 const contextMenus = {
@@ -37,12 +38,21 @@ const i18n = {
 const tabs = {
   executeScript: jest.fn(),
   sendMessage: jest.fn(),
+  query: jest.fn(),
 };
 
 const scripting = {
   executeScript: jest.fn(),
 };
 
+const windows = {
+  create: jest.fn(),
+  get: jest.fn(),
+  getCurrent: jest.fn(),
+  update: jest.fn(),
+  remove: jest.fn(),
+};
+
 // set chrome
 global.chrome = {
   i18n,
@@ -51,4 +61,5 @@ global.chrome = {
   contextMenus,
   tabs,
   scripting,
+  windows,
 } as any;