diff --git a/apps/browser/src/_locales/en/messages.json b/apps/browser/src/_locales/en/messages.json
index b5d5afb27c4..63dd227e52b 100644
--- a/apps/browser/src/_locales/en/messages.json
+++ b/apps/browser/src/_locales/en/messages.json
@@ -630,6 +630,12 @@
   "notificationChangeSave": {
     "message": "Update"
   },
+  "notificationUnlockDesc": {
+    "message": "Unlock your Bitwarden vault to complete the auto-fill request."
+  },
+  "notificationUnlock": {
+    "message": "Unlock"
+  },
   "enableContextMenuItem": {
     "message": "Show context menu options"
   },
diff --git a/apps/browser/src/autofill/background/context-menus.background.ts b/apps/browser/src/autofill/background/context-menus.background.ts
index 681f86cdf67..bc26353cbd9 100644
--- a/apps/browser/src/autofill/background/context-menus.background.ts
+++ b/apps/browser/src/autofill/background/context-menus.background.ts
@@ -30,6 +30,7 @@ export default class ContextMenusBackground {
             msg.data.commandToRetry.msg.data,
             msg.data.commandToRetry.sender.tab
           );
+          await BrowserApi.tabSendMessageData(sender.tab, "closeNotificationBar");
         }
       }
     );
diff --git a/apps/browser/src/autofill/background/notification.background.ts b/apps/browser/src/autofill/background/notification.background.ts
index 07b565e2608..1cb006fa3a2 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 AddUnlockVaultQueueMessage from "../../background/models/add-unlock-vault-queue-message";
 import AddChangePasswordQueueMessage from "../../background/models/addChangePasswordQueueMessage";
 import AddLoginQueueMessage from "../../background/models/addLoginQueueMessage";
 import AddLoginRuntimeMessage from "../../background/models/addLoginRuntimeMessage";
@@ -23,7 +24,11 @@ import { BrowserStateService } from "../../platform/services/abstractions/browse
 import { AutofillService } from "../services/abstractions/autofill.service";
 
 export default class NotificationBackground {
-  private notificationQueue: (AddLoginQueueMessage | AddChangePasswordQueueMessage)[] = [];
+  private notificationQueue: (
+    | AddLoginQueueMessage
+    | AddChangePasswordQueueMessage
+    | AddUnlockVaultQueueMessage
+  )[] = [];
 
   constructor(
     private autofillService: AutofillService,
@@ -53,10 +58,7 @@ export default class NotificationBackground {
   async processMessage(msg: any, sender: chrome.runtime.MessageSender) {
     switch (msg.command) {
       case "unlockCompleted":
-        if (msg.data.target !== "notification.background") {
-          return;
-        }
-        await this.processMessage(msg.data.commandToRetry.msg, msg.data.commandToRetry.sender);
+        await this.handleUnlockCompleted(msg.data, sender);
         break;
       case "bgGetDataForTab":
         await this.getDataForTab(sender.tab, msg.responseCommand);
@@ -82,7 +84,9 @@ export default class NotificationBackground {
         if ((await this.authService.getAuthStatus()) < AuthenticationStatus.Unlocked) {
           const retryMessage: LockedVaultPendingNotificationsItem = {
             commandToRetry: {
-              msg: msg,
+              msg: {
+                command: msg,
+              },
               sender: sender,
             },
             target: "notification.background",
@@ -114,6 +118,9 @@ export default class NotificationBackground {
             break;
         }
         break;
+      case "promptForLogin":
+        await this.unlockVault(sender.tab);
+        break;
       default:
         break;
     }
@@ -181,6 +188,14 @@ export default class NotificationBackground {
             webVaultURL: await this.environmentService.getWebVaultUrl(),
           },
         });
+      } else if (this.notificationQueue[i].type === NotificationQueueMessageType.UnlockVault) {
+        BrowserApi.tabSendMessageData(tab, "openNotificationBar", {
+          type: "unlock",
+          typeData: {
+            isVaultLocked: this.notificationQueue[i].wasVaultLocked,
+            theme: await this.getCurrentTheme(),
+          },
+        });
       }
       break;
     }
@@ -305,6 +320,20 @@ export default class NotificationBackground {
     }
   }
 
+  private async unlockVault(tab: chrome.tabs.Tab) {
+    const currentAuthStatus = await this.authService.getAuthStatus();
+    if (currentAuthStatus !== AuthenticationStatus.Locked || this.notificationQueue.length) {
+      return;
+    }
+
+    const loginDomain = Utils.getDomain(tab.url);
+    if (!loginDomain) {
+      return;
+    }
+
+    this.pushUnlockVaultToQueue(loginDomain, tab);
+  }
+
   private async pushChangePasswordToQueue(
     cipherId: string,
     loginDomain: string,
@@ -327,6 +356,20 @@ export default class NotificationBackground {
     await this.checkNotificationQueue(tab);
   }
 
+  private async pushUnlockVaultToQueue(loginDomain: string, tab: chrome.tabs.Tab) {
+    this.removeTabFromNotificationQueue(tab);
+    const message: AddUnlockVaultQueueMessage = {
+      type: NotificationQueueMessageType.UnlockVault,
+      domain: loginDomain,
+      tabId: tab.id,
+      expires: new Date(new Date().getTime() + 0.5 * 60000), // 30 seconds
+      wasVaultLocked: true,
+    };
+    this.notificationQueue.push(message);
+    await this.checkNotificationQueue(tab);
+    this.removeTabFromNotificationQueue(tab);
+  }
+
   private async saveOrUpdateCredentials(tab: chrome.tabs.Tab, edit: boolean, folderId?: string) {
     for (let i = this.notificationQueue.length - 1; i >= 0; i--) {
       const queueMessage = this.notificationQueue[i];
@@ -463,4 +506,22 @@ export default class NotificationBackground {
       this.policyService.policyAppliesToActiveUser$(PolicyType.PersonalOwnership)
     );
   }
+
+  private async handleUnlockCompleted(
+    messageData: LockedVaultPendingNotificationsItem,
+    sender: chrome.runtime.MessageSender
+  ): Promise<void> {
+    if (messageData.commandToRetry.msg.command === "autofill_login") {
+      await BrowserApi.tabSendMessageData(sender.tab, "closeNotificationBar");
+    }
+
+    if (messageData.target !== "notification.background") {
+      return;
+    }
+
+    await this.processMessage(
+      messageData.commandToRetry.msg.command,
+      messageData.commandToRetry.sender
+    );
+  }
 }
diff --git a/apps/browser/src/autofill/notification/bar.html b/apps/browser/src/autofill/notification/bar.html
index deec7fd512c..a6be58de70a 100644
--- a/apps/browser/src/autofill/notification/bar.html
+++ b/apps/browser/src/autofill/notification/bar.html
@@ -51,4 +51,13 @@
       </div>
     </div>
   </template>
+
+  <template id="template-unlock">
+    <div class="inner-wrapper">
+      <div id="unlock-text"></div>
+      <div>
+        <button type="button" id="unlock-vault" class="primary"></button>
+      </div>
+    </div>
+  </template>
 </html>
diff --git a/apps/browser/src/autofill/notification/bar.ts b/apps/browser/src/autofill/notification/bar.ts
index 728ae4e1287..dcc4ce010f6 100644
--- a/apps/browser/src/autofill/notification/bar.ts
+++ b/apps/browser/src/autofill/notification/bar.ts
@@ -28,6 +28,8 @@ function load() {
     notificationEdit: chrome.i18n.getMessage("edit"),
     notificationChangeSave: chrome.i18n.getMessage("notificationChangeSave"),
     notificationChangeDesc: chrome.i18n.getMessage("notificationChangeDesc"),
+    notificationUnlock: chrome.i18n.getMessage("notificationUnlock"),
+    notificationUnlockDesc: chrome.i18n.getMessage("notificationUnlockDesc"),
   };
 
   const logoLink = document.getElementById("logo-link") as HTMLAnchorElement;
@@ -72,6 +74,13 @@ function load() {
 
   changeTemplate.content.getElementById("change-text").textContent = i18n.notificationChangeDesc;
 
+  const unlockTemplate = document.getElementById("template-unlock") as HTMLTemplateElement;
+
+  const unlockButton = unlockTemplate.content.getElementById("unlock-vault");
+  unlockButton.textContent = i18n.notificationUnlock;
+
+  unlockTemplate.content.getElementById("unlock-text").textContent = i18n.notificationUnlockDesc;
+
   // i18n for body content
   const closeButton = document.getElementById("close-button");
   closeButton.title = i18n.close;
@@ -80,6 +89,8 @@ function load() {
     handleTypeAdd();
   } else if (getQueryVariable("type") === "change") {
     handleTypeChange();
+  } else if (getQueryVariable("type") === "unlock") {
+    handleTypeUnlock();
   }
 
   closeButton.addEventListener("click", (e) => {
@@ -172,6 +183,17 @@ function handleTypeChange() {
   });
 }
 
+function handleTypeUnlock() {
+  setContent(document.getElementById("template-unlock") as HTMLTemplateElement);
+
+  const unlockButton = document.getElementById("unlock-vault");
+  unlockButton.addEventListener("click", (e) => {
+    sendPlatformMessage({
+      command: "bgReopenPromptForLogin",
+    });
+  });
+}
+
 function setContent(template: HTMLTemplateElement) {
   const content = document.getElementById("content");
   while (content.firstChild) {
diff --git a/apps/browser/src/background/main.background.ts b/apps/browser/src/background/main.background.ts
index 4e310354699..59a1b444e09 100644
--- a/apps/browser/src/background/main.background.ts
+++ b/apps/browser/src/background/main.background.ts
@@ -114,6 +114,7 @@ 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 { BrowserCryptoService } from "../platform/services/browser-crypto.service";
 import { BrowserEnvironmentService } from "../platform/services/browser-environment.service";
@@ -195,6 +196,7 @@ export default class MainBackground {
   cipherContextMenuHandler: CipherContextMenuHandler;
   configService: ConfigServiceAbstraction;
   configApiService: ConfigApiServiceAbstraction;
+  browserPopoutWindowService: BrowserPopoutWindowService;
 
   // Passed to the popup for Safari to workaround issues with theming, downloading, etc.
   backgroundWindow = window;
@@ -512,6 +514,7 @@ export default class MainBackground {
       this.authService,
       this.environmentService
     );
+    this.browserPopoutWindowService = new BrowserPopoutWindowService();
 
     const systemUtilsServiceReloadCallback = () => {
       const forceWindowReload =
@@ -543,7 +546,8 @@ export default class MainBackground {
       this.environmentService,
       this.messagingService,
       this.logService,
-      this.configService
+      this.configService,
+      this.browserPopoutWindowService
     );
     this.nativeMessagingBackground = new NativeMessagingBackground(
       this.cryptoService,
diff --git a/apps/browser/src/background/models/add-unlock-vault-queue-message.ts b/apps/browser/src/background/models/add-unlock-vault-queue-message.ts
new file mode 100644
index 00000000000..9ddde271008
--- /dev/null
+++ b/apps/browser/src/background/models/add-unlock-vault-queue-message.ts
@@ -0,0 +1,6 @@
+import NotificationQueueMessage from "./notificationQueueMessage";
+import { NotificationQueueMessageType } from "./notificationQueueMessageType";
+
+export default class AddUnlockVaultQueueMessage extends NotificationQueueMessage {
+  type: NotificationQueueMessageType.UnlockVault;
+}
diff --git a/apps/browser/src/background/models/lockedVaultPendingNotificationsItem.ts b/apps/browser/src/background/models/lockedVaultPendingNotificationsItem.ts
index ec697b16994..53f8405cd50 100644
--- a/apps/browser/src/background/models/lockedVaultPendingNotificationsItem.ts
+++ b/apps/browser/src/background/models/lockedVaultPendingNotificationsItem.ts
@@ -1,6 +1,9 @@
 export default class LockedVaultPendingNotificationsItem {
   commandToRetry: {
-    msg: any;
+    msg: {
+      command: string;
+      data?: any;
+    };
     sender: chrome.runtime.MessageSender;
   };
   target: string;
diff --git a/apps/browser/src/background/models/notificationQueueMessageType.ts b/apps/browser/src/background/models/notificationQueueMessageType.ts
index f5e4115c4f5..2ce1a1840d8 100644
--- a/apps/browser/src/background/models/notificationQueueMessageType.ts
+++ b/apps/browser/src/background/models/notificationQueueMessageType.ts
@@ -1,4 +1,5 @@
 export enum NotificationQueueMessageType {
   AddLogin = 0,
   ChangePassword = 1,
+  UnlockVault = 2,
 }
diff --git a/apps/browser/src/background/runtime.background.ts b/apps/browser/src/background/runtime.background.ts
index 81f7376a94d..2e9fc934882 100644
--- a/apps/browser/src/background/runtime.background.ts
+++ b/apps/browser/src/background/runtime.background.ts
@@ -8,6 +8,7 @@ import { Utils } from "@bitwarden/common/platform/misc/utils";
 
 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 { BrowserEnvironmentService } from "../platform/services/browser-environment.service";
 import BrowserPlatformUtilsService from "../platform/services/browser-platform-utils.service";
 
@@ -30,7 +31,8 @@ export default class RuntimeBackground {
     private environmentService: BrowserEnvironmentService,
     private messagingService: MessagingService,
     private logService: LogService,
-    private configService: ConfigServiceAbstraction
+    private configService: ConfigServiceAbstraction,
+    private browserPopoutWindowService: BrowserPopoutWindowService
   ) {
     // onInstalled listener must be wired up before anything else, so we do it in the ctor
     chrome.runtime.onInstalled.addListener((details: any) => {
@@ -66,7 +68,7 @@ export default class RuntimeBackground {
 
         if (this.lockedVaultPendingNotifications?.length > 0) {
           item = this.lockedVaultPendingNotifications.pop();
-          BrowserApi.closeBitwardenExtensionTab();
+          await this.browserPopoutWindowService.closeLoginPrompt();
         }
 
         await this.main.refreshBadge();
@@ -105,7 +107,8 @@ export default class RuntimeBackground {
         await this.main.openPopup();
         break;
       case "promptForLogin":
-        BrowserApi.openBitwardenExtensionTab("popup/index.html", true);
+      case "bgReopenPromptForLogin":
+        await this.browserPopoutWindowService.openLoginPrompt(sender.tab?.windowId);
         break;
       case "openAddEditCipher": {
         const addEditCipherUrl =
diff --git a/apps/browser/src/platform/browser/browser-api.ts b/apps/browser/src/platform/browser/browser-api.ts
index 7c646e5c7e6..243971dbfc0 100644
--- a/apps/browser/src/platform/browser/browser-api.ts
+++ b/apps/browser/src/platform/browser/browser-api.ts
@@ -17,6 +17,24 @@ export class BrowserApi {
     return chrome.runtime.getManifest().manifest_version;
   }
 
+  static getWindow(windowId?: number): Promise<chrome.windows.Window> | void {
+    if (!windowId) {
+      return;
+    }
+
+    return new Promise((resolve) =>
+      chrome.windows.get(windowId, { populate: true }, (window) => resolve(window))
+    );
+  }
+
+  static async createWindow(options: chrome.windows.CreateData): Promise<chrome.windows.Window> {
+    return new Promise((resolve) =>
+      chrome.windows.create(options, (window) => {
+        resolve(window);
+      })
+    );
+  }
+
   static async getTabFromCurrentWindowId(): Promise<chrome.tabs.Tab> | null {
     return await BrowserApi.tabsQueryFirst({
       active: true,
@@ -105,6 +123,10 @@ 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);
   }
@@ -165,7 +187,7 @@ export class BrowserApi {
     }
 
     const tabToClose = tabs[tabs.length - 1];
-    chrome.tabs.remove(tabToClose.id);
+    BrowserApi.removeTab(tabToClose.id);
   }
 
   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
new file mode 100644
index 00000000000..ca22e369d80
--- /dev/null
+++ b/apps/browser/src/platform/popup/abstractions/browser-popout-window.service.ts
@@ -0,0 +1,6 @@
+interface BrowserPopoutWindowService {
+  openLoginPrompt(senderWindowId: number): Promise<void>;
+  closeLoginPrompt(): Promise<void>;
+}
+
+export { BrowserPopoutWindowService };
diff --git a/apps/browser/src/platform/popup/browser-popout-window.service.ts b/apps/browser/src/platform/popup/browser-popout-window.service.ts
new file mode 100644
index 00000000000..bfec3e690ba
--- /dev/null
+++ b/apps/browser/src/platform/popup/browser-popout-window.service.ts
@@ -0,0 +1,64 @@
+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: "normal",
+    focused: true,
+    width: 500,
+    height: 800,
+  };
+
+  async openLoginPrompt(senderWindowId: number) {
+    await this.closeLoginPrompt();
+    await this.openPopoutWindow(
+      senderWindowId,
+      "popup/index.html?uilocation=popout",
+      "loginPrompt"
+    );
+  }
+
+  async closeLoginPrompt() {
+    await this.closeSingleActionPopout("loginPrompt");
+  }
+
+  private async openPopoutWindow(
+    senderWindowId: number,
+    popupWindowURL: string,
+    singleActionPopoutKey: string
+  ) {
+    const senderWindow = senderWindowId && (await BrowserApi.getWindow(senderWindowId));
+    const url = chrome.extension.getURL(popupWindowURL);
+    const offsetRight = 15;
+    const offsetTop = 90;
+    const popupWidth = this.defaultPopoutWindowOptions.width;
+    const windowOptions = senderWindow
+      ? {
+          ...this.defaultPopoutWindowOptions,
+          url,
+          left: senderWindow.left + senderWindow.width - popupWidth - offsetRight,
+          top: senderWindow.top + offsetTop,
+        }
+      : { ...this.defaultPopoutWindowOptions, url };
+
+    const popupWindow = await BrowserApi.createWindow(windowOptions);
+
+    if (!singleActionPopoutKey) {
+      return;
+    }
+    this.singleActionPopoutTabIds[singleActionPopoutKey] = popupWindow?.tabs[0].id;
+  }
+
+  private async closeSingleActionPopout(popoutKey: string) {
+    const tabId = this.singleActionPopoutTabIds[popoutKey];
+    if (!tabId) {
+      return;
+    }
+    await BrowserApi.removeTab(tabId);
+    this.singleActionPopoutTabIds[popoutKey] = null;
+  }
+}
+
+export default BrowserPopoutWindowService;