diff --git a/apps/browser/src/background/main.background.ts b/apps/browser/src/background/main.background.ts
index c4c412732c9..bcceac6fb84 100644
--- a/apps/browser/src/background/main.background.ts
+++ b/apps/browser/src/background/main.background.ts
@@ -300,6 +300,7 @@ import { BrowserActionsService } from "../platform/actions/browser-actions.servi
 import { DefaultBadgeBrowserApi } from "../platform/badge/badge-browser-api";
 import { BadgeService } from "../platform/badge/badge.service";
 import { BrowserApi } from "../platform/browser/browser-api";
+import BrowserPopupUtils from "../platform/browser/browser-popup-utils";
 import { flagEnabled } from "../platform/flags";
 import { IpcBackgroundService } from "../platform/ipc/ipc-background.service";
 import { IpcContentScriptManagerService } from "../platform/ipc/ipc-content-script-manager.service";
@@ -1237,6 +1238,12 @@ export default class MainBackground {
 
     const systemUtilsServiceReloadCallback = async () => {
       await this.taskSchedulerService.clearAllScheduledTasks();
+
+      // Close browser action popup before reloading to prevent zombie popup with invalidated context.
+      // The 'reloadProcess' message is sent by ProcessReloadService before this callback runs,
+      // and popups will close themselves upon receiving it. Poll to verify popup is actually closed.
+      await BrowserPopupUtils.waitForAllPopupsClose();
+
       BrowserApi.reloadExtension();
     };
 
diff --git a/apps/browser/src/platform/browser/browser-popup-utils.spec.ts b/apps/browser/src/platform/browser/browser-popup-utils.spec.ts
index 9f9a6e313c8..e4165348c6e 100644
--- a/apps/browser/src/platform/browser/browser-popup-utils.spec.ts
+++ b/apps/browser/src/platform/browser/browser-popup-utils.spec.ts
@@ -337,6 +337,68 @@ describe("BrowserPopupUtils", () => {
     });
   });
 
+  describe("waitForAllPopupsClose", () => {
+    beforeEach(() => {
+      jest.useFakeTimers();
+    });
+
+    afterEach(() => {
+      jest.useRealTimers();
+    });
+
+    it("should resolve immediately if no popups are open", async () => {
+      jest.spyOn(BrowserApi, "isPopupOpen").mockResolvedValue(false);
+
+      const promise = BrowserPopupUtils.waitForAllPopupsClose();
+      jest.advanceTimersByTime(100);
+
+      await expect(promise).resolves.toBeUndefined();
+      expect(BrowserApi.isPopupOpen).toHaveBeenCalledTimes(1);
+    });
+
+    it("should resolve after timeout if popup never closes when using custom timeout", async () => {
+      jest.spyOn(BrowserApi, "isPopupOpen").mockResolvedValue(true);
+
+      const promise = BrowserPopupUtils.waitForAllPopupsClose(500);
+
+      // Advance past the timeout
+      jest.advanceTimersByTime(600);
+
+      await expect(promise).resolves.toBeUndefined();
+    });
+
+    it("should resolve after timeout if popup never closes when using default timeout", async () => {
+      jest.spyOn(BrowserApi, "isPopupOpen").mockResolvedValue(true);
+
+      const promise = BrowserPopupUtils.waitForAllPopupsClose();
+
+      // Advance past the default timeout
+      jest.advanceTimersByTime(1100);
+
+      await expect(promise).resolves.toBeUndefined();
+    });
+
+    it("should stop polling after popup closes before timeout", async () => {
+      let callCount = 0;
+      jest.spyOn(BrowserApi, "isPopupOpen").mockImplementation(async () => {
+        callCount++;
+        return callCount <= 2;
+      });
+
+      const promise = BrowserPopupUtils.waitForAllPopupsClose(1000);
+
+      // Advance to when popup closes (300ms)
+      jest.advanceTimersByTime(300);
+
+      await expect(promise).resolves.toBeUndefined();
+
+      // Advance further to ensure no more calls are made
+      jest.advanceTimersByTime(1000);
+
+      expect(BrowserApi.isPopupOpen).toHaveBeenCalledTimes(3);
+    });
+  });
+
   describe("isSingleActionPopoutOpen", () => {
     const windowOptions = {
       id: 1,
diff --git a/apps/browser/src/platform/browser/browser-popup-utils.ts b/apps/browser/src/platform/browser/browser-popup-utils.ts
index aebb3e92113..cd55f6361a0 100644
--- a/apps/browser/src/platform/browser/browser-popup-utils.ts
+++ b/apps/browser/src/platform/browser/browser-popup-utils.ts
@@ -1,5 +1,6 @@
 // FIXME: Update this file to be type safe and remove this and next line
 // @ts-strict-ignore
+import { filter, firstValueFrom, interval, of, switchMap, takeWhile, timeout } from "rxjs";
 
 import { ScrollOptions } from "./abstractions/browser-popup-utils.abstractions";
 import { BrowserApi } from "./browser-api";
@@ -212,6 +213,27 @@ export default class BrowserPopupUtils {
     }
   }
 
+  /**
+   * Waits for all browser action popups to close, polling up to the specified timeout.
+   * Used before extension reload to prevent zombie popups with invalidated contexts.
+   *
+   * @param timeoutMs - Maximum time to wait in milliseconds. Defaults to 1 second.
+   * @returns Promise that resolves when all popups are closed or timeout is reached.
+   */
+  static async waitForAllPopupsClose(timeoutMs = 1000): Promise<void> {
+    await firstValueFrom(
+      interval(100).pipe(
+        switchMap(() => BrowserApi.isPopupOpen()),
+        takeWhile((isOpen) => isOpen, true),
+        filter((isOpen) => !isOpen),
+        timeout({
+          first: timeoutMs,
+          with: () => of(true),
+        }),
+      ),
+    );
+  }
+
   /**
    * 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
diff --git a/apps/browser/src/popup/app.component.ts b/apps/browser/src/popup/app.component.ts
index 998531488d3..b85da665fa0 100644
--- a/apps/browser/src/popup/app.component.ts
+++ b/apps/browser/src/popup/app.component.ts
@@ -36,6 +36,7 @@ import {
   LogoutReason,
   UserDecryptionOptionsServiceAbstraction,
 } from "@bitwarden/auth/common";
+import { BrowserApi } from "@bitwarden/browser/platform/browser/browser-api";
 import { AccountService } from "@bitwarden/common/auth/abstractions/account.service";
 import { AuthRequestAnsweringServiceAbstraction } from "@bitwarden/common/auth/abstractions/auth-request-answering/auth-request-answering.service.abstraction";
 import { AuthService } from "@bitwarden/common/auth/abstractions/auth.service";
@@ -58,6 +59,7 @@ import {
 } from "@bitwarden/components";
 import { BiometricsService, BiometricStateService, KeyService } from "@bitwarden/key-management";
 
+import BrowserPopupUtils from "../platform/browser/browser-popup-utils";
 import { PopupCompactModeService } from "../platform/popup/layout/popup-compact-mode.service";
 import { PopupSizeService } from "../platform/popup/layout/popup-size.service";
 import { initPopupClosedListener } from "../platform/services/popup-view-cache-background.service";
@@ -286,6 +288,13 @@ export class AppComponent implements OnInit, OnDestroy {
                 await this.biometricStateService.updateLastProcessReload();
                 window.location.reload();
               }, 2000);
+            } else {
+              // Close browser action popup before extension reload to prevent zombie popup with invalidated context.
+              // This issue occurs in Chromium-based browsers (Chrome, Vivaldi, etc.) where chrome.runtime.reload()
+              // invalidates extension contexts before popup can close naturally
+              if (BrowserPopupUtils.inPopup(window)) {
+                BrowserApi.closePopup(window);
+              }
             }
           } else if (msg.command === "reloadPopup") {
             // FIXME: Verify that this floating promise is intentional. If it is, add an explanatory comment and ensure there is proper error handling.