diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index b0bd5f2246..27b7ff1163 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -12,10 +12,10 @@ type PageDetailsForTab = Record<
 >;
 
 type SubFrameOffsetData = {
+  frameId?: number;
   url?: string;
   top: number;
   left: number;
-  frameId?: number;
 } | null;
 
 type SubFrameOffsetsForTab = Record<
@@ -49,9 +49,9 @@ type OverlayBackgroundExtensionMessage = {
   forceCloseOverlay?: boolean;
   isOverlayHidden?: boolean;
   setTransparentOverlay?: boolean;
-  data?: LockedVaultPendingNotificationsData;
   isFieldCurrentlyFocused?: boolean;
   isCurrentlyFilling?: boolean;
+  data?: LockedVaultPendingNotificationsData;
 } & OverlayAddNewItemMessage;
 
 type OverlayPortMessage = {
@@ -132,6 +132,7 @@ type OverlayButtonPortMessageHandlers = {
   forceCloseAutofillOverlay: ({ port }: PortConnectionParam) => void;
   overlayPageBlurred: () => void;
   redirectOverlayFocusOut: ({ message, port }: PortOnMessageHandlerParams) => void;
+  getPageColorScheme: () => void;
 };
 
 type OverlayListPortMessageHandlers = {
@@ -144,6 +145,7 @@ type OverlayListPortMessageHandlers = {
   addNewVaultItem: ({ port }: PortConnectionParam) => void;
   viewSelectedCipher: ({ message, port }: PortOnMessageHandlerParams) => void;
   redirectOverlayFocusOut: ({ message, port }: PortOnMessageHandlerParams) => void;
+  updateAutofillOverlayListHeight: ({ message, port }: PortOnMessageHandlerParams) => void;
 };
 
 interface OverlayBackground {
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index e96a5106ab..3f54340f10 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -95,6 +95,11 @@ class OverlayBackground implements OverlayBackgroundInterface {
       this.closeOverlay(port.sender, { forceCloseOverlay: true }),
     overlayPageBlurred: () => this.checkOverlayListFocused(),
     redirectOverlayFocusOut: ({ message, port }) => this.redirectOverlayFocusOut(message, port),
+    getPageColorScheme: () => {
+      this.overlayButtonPort?.postMessage({
+        command: "getPageColorScheme",
+      });
+    },
   };
   private readonly overlayListPortMessageHandlers: OverlayListPortMessageHandlers = {
     checkAutofillOverlayButtonFocused: () => this.checkOverlayButtonFocused(),
@@ -106,6 +111,12 @@ class OverlayBackground implements OverlayBackgroundInterface {
     addNewVaultItem: ({ port }) => this.getNewVaultItemDetails(port),
     viewSelectedCipher: ({ message, port }) => this.viewSelectedCipher(message, port),
     redirectOverlayFocusOut: ({ message, port }) => this.redirectOverlayFocusOut(message, port),
+    updateAutofillOverlayListHeight: ({ message }) => {
+      this.overlayListPort?.postMessage({
+        command: "updateIframePosition",
+        styles: message.styles,
+      });
+    },
   };
 
   constructor(
@@ -832,7 +843,7 @@ class OverlayBackground implements OverlayBackgroundInterface {
     await BrowserApi.sendMessage("inlineAutofillMenuRefreshAddEditCipher");
   }
 
-  private updateIsFieldCurrentlyFocused({ message }: OverlayBackgroundExtensionMessage) {
+  private updateIsFieldCurrentlyFocused(message: OverlayBackgroundExtensionMessage) {
     this.isFieldCurrentlyFocused = message.isFieldCurrentlyFocused;
   }
 
@@ -910,6 +921,14 @@ class OverlayBackground implements OverlayBackgroundInterface {
    * @param port - The port that connected to the extension background
    */
   private handlePortOnConnect = async (port: chrome.runtime.Port) => {
+    const isOverlayListMessageConnector = port.name === AutofillOverlayPort.ListMessageConnector;
+    const isOverlayButtonMessageConnector =
+      port.name === AutofillOverlayPort.ButtonMessageConnector;
+    if (isOverlayListMessageConnector || isOverlayButtonMessageConnector) {
+      port.onMessage.addListener(this.handleOverlayElementPortMessage);
+      return;
+    }
+
     const isOverlayListPort = port.name === AutofillOverlayPort.List;
     const isOverlayButtonPort = port.name === AutofillOverlayPort.Button;
 
@@ -923,7 +942,6 @@ class OverlayBackground implements OverlayBackgroundInterface {
       this.overlayButtonPort = port;
     }
 
-    port.onMessage.addListener(this.handleOverlayElementPortMessage);
     port.onDisconnect.addListener(this.handlePortOnDisconnect);
     port.postMessage({
       command: `initAutofillOverlay${isOverlayListPort ? "List" : "Button"}`,
@@ -932,6 +950,7 @@ class OverlayBackground implements OverlayBackgroundInterface {
       theme: await firstValueFrom(this.themeStateService.selectedTheme$),
       translations: this.getTranslations(),
       ciphers: isOverlayListPort ? await this.getOverlayCipherData() : null,
+      messageConnectorUrl: chrome.runtime.getURL("overlay/message-connector.html"),
     });
     void this.updateOverlayPosition(
       {
@@ -956,11 +975,11 @@ class OverlayBackground implements OverlayBackgroundInterface {
     const command = message?.command;
     let handler: CallableFunction | undefined;
 
-    if (port.name === AutofillOverlayPort.Button) {
+    if (port.name === AutofillOverlayPort.ButtonMessageConnector) {
       handler = this.overlayButtonPortMessageHandlers[command];
     }
 
-    if (port.name === AutofillOverlayPort.List) {
+    if (port.name === AutofillOverlayPort.ListMessageConnector) {
       handler = this.overlayListPortMessageHandlers[command];
     }
 
diff --git a/apps/browser/src/autofill/notification/bar.ts b/apps/browser/src/autofill/notification/bar.ts
index a730ee1eba..61ea034fb0 100644
--- a/apps/browser/src/autofill/notification/bar.ts
+++ b/apps/browser/src/autofill/notification/bar.ts
@@ -24,7 +24,7 @@ const notificationBarWindowMessageHandlers: NotificationBarWindowMessageHandlers
 globalThis.addEventListener("load", load);
 function load() {
   setupWindowMessageListener();
-  postMessageToParent({ command: "initNotificationBar" });
+  postMessageToConnector({ command: "initNotificationBar" });
 }
 
 function initNotificationBar(message: NotificationBarWindowMessage) {
@@ -392,6 +392,6 @@ function setNotificationBarTheme() {
   document.documentElement.classList.add(`theme_${theme}`);
 }
 
-function postMessageToParent(message: NotificationBarWindowMessage) {
+function postMessageToConnector(message: NotificationBarWindowMessage) {
   globalThis.parent.postMessage(message, windowMessageOrigin || "*");
 }
diff --git a/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-button.ts b/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-button.ts
index b6b22be943..3fa34693d3 100644
--- a/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-button.ts
+++ b/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-button.ts
@@ -7,6 +7,7 @@ type UpdateAuthStatusMessage = OverlayButtonMessage & { authStatus: Authenticati
 type InitAutofillOverlayButtonMessage = UpdateAuthStatusMessage & {
   styleSheetUrl: string;
   translations: Record<string, string>;
+  messageConnectorUrl: string;
 };
 
 type OverlayButtonWindowMessageHandlers = {
diff --git a/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-iframe.service.ts b/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-iframe.service.ts
index 0c4160a070..2357ca2b8f 100644
--- a/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-iframe.service.ts
+++ b/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-iframe.service.ts
@@ -7,7 +7,6 @@ type AutofillOverlayIframeExtensionMessage = {
 type AutofillOverlayIframeWindowMessageHandlers = {
   [key: string]: CallableFunction;
   updateAutofillOverlayListHeight: (message: AutofillOverlayIframeExtensionMessage) => void;
-  getPageColorScheme: () => void;
 };
 
 type AutofillOverlayIframeExtensionMessageParam = {
@@ -19,6 +18,7 @@ type BackgroundPortMessageHandlers = {
   initAutofillOverlayList: ({ message }: AutofillOverlayIframeExtensionMessageParam) => void;
   updateIframePosition: ({ message }: AutofillOverlayIframeExtensionMessageParam) => void;
   updateOverlayHidden: ({ message }: AutofillOverlayIframeExtensionMessageParam) => void;
+  getPageColorScheme: () => void;
 };
 
 interface AutofillOverlayIframeService {
diff --git a/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-list.ts b/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-list.ts
index b656f238dc..ce49d5c85c 100644
--- a/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-list.ts
+++ b/apps/browser/src/autofill/overlay/abstractions/autofill-overlay-list.ts
@@ -14,6 +14,7 @@ type InitAutofillOverlayListMessage = OverlayListMessage & {
   theme: string;
   translations: Record<string, string>;
   ciphers?: OverlayCipherData[];
+  messageConnectorUrl: string;
 };
 
 type OverlayListWindowMessageHandlers = {
diff --git a/apps/browser/src/autofill/overlay/content/inline-menu-elements.ts b/apps/browser/src/autofill/overlay/content/inline-menu-elements.ts
index 9b0cbf4e9a..64298802f4 100644
--- a/apps/browser/src/autofill/overlay/content/inline-menu-elements.ts
+++ b/apps/browser/src/autofill/overlay/content/inline-menu-elements.ts
@@ -70,13 +70,13 @@ export class InlineMenuElements implements InlineMenuElementsInterface {
    * unobserve the body element to ensure the mutation observer no
    * longer triggers.
    */
-  private removeInlineMenu = (message: any) => {
-    if (message.overlayElement === AutofillOverlayElement.Button) {
+  private removeInlineMenu = (message?: AutofillExtensionMessage) => {
+    if (message?.overlayElement === AutofillOverlayElement.Button) {
       this.removeInlineMenuButton();
       return;
     }
 
-    if (message.overlayElement === AutofillOverlayElement.List) {
+    if (message?.overlayElement === AutofillOverlayElement.List) {
       this.removeInlineMenuList();
       return;
     }
@@ -408,7 +408,7 @@ export class InlineMenuElements implements InlineMenuElementsInterface {
       clearTimeout(this.mutationObserverIterationsResetTimeout);
       this.mutationObserverIterations = 0;
       void this.sendExtensionMessage("blurMostRecentOverlayField");
-      this.removeInlineMenu({ forceClose: true });
+      this.removeInlineMenu();
 
       return true;
     }
@@ -417,6 +417,6 @@ export class InlineMenuElements implements InlineMenuElementsInterface {
   }
   destroy() {
     this.documentElementMutationObserver?.disconnect();
-    this.removeInlineMenu({ forceClose: true });
+    this.removeInlineMenu();
   }
 }
diff --git a/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts b/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts
index b7a6f2a39e..7bfa676d53 100644
--- a/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts
+++ b/apps/browser/src/autofill/overlay/iframe-content/autofill-overlay-iframe.service.ts
@@ -1,17 +1,15 @@
 import { EVENTS } from "@bitwarden/common/autofill/constants";
 import { ThemeType } from "@bitwarden/common/platform/enums";
 
-import { setElementStyles } from "../../utils";
+import { sendExtensionMessage, setElementStyles } from "../../utils";
 import {
   BackgroundPortMessageHandlers,
   AutofillOverlayIframeService as AutofillOverlayIframeServiceInterface,
   AutofillOverlayIframeExtensionMessage,
-  AutofillOverlayIframeWindowMessageHandlers,
 } from "../abstractions/autofill-overlay-iframe.service";
 
 class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterface {
   private port: chrome.runtime.Port | null = null;
-  private extensionOriginsSet: Set<string>;
   private iframeMutationObserver: MutationObserver;
   private iframe: HTMLIFrameElement;
   private ariaAlertElement: HTMLDivElement;
@@ -42,15 +40,11 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
   private foreignMutationsCount = 0;
   private mutationObserverIterations = 0;
   private mutationObserverIterationsResetTimeout: number | NodeJS.Timeout;
-  private readonly windowMessageHandlers: AutofillOverlayIframeWindowMessageHandlers = {
-    updateAutofillOverlayListHeight: (message) =>
-      this.updateElementStyles(this.iframe, message.styles),
-    getPageColorScheme: () => this.updateOverlayPageColorScheme(),
-  };
   private readonly backgroundPortMessageHandlers: BackgroundPortMessageHandlers = {
     initAutofillOverlayList: ({ message }) => this.initAutofillOverlayList(message),
     updateIframePosition: ({ message }) => this.updateIframePosition(message.styles),
     updateOverlayHidden: ({ message }) => this.updateElementStyles(this.iframe, message.styles),
+    getPageColorScheme: () => this.updateOverlayPageColorScheme(),
   };
 
   constructor(
@@ -58,11 +52,6 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
     private portName: string,
     private shadow: ShadowRoot,
   ) {
-    this.extensionOriginsSet = new Set([
-      chrome.runtime.getURL("").slice(0, -1).toLowerCase(), // Remove the trailing slash and normalize the extension url to lowercase
-      "null",
-    ]);
-
     this.iframeMutationObserver = new MutationObserver(this.handleMutations);
   }
 
@@ -134,7 +123,6 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
     this.port = chrome.runtime.connect({ name: this.portName });
     this.port.onDisconnect.addListener(this.handlePortDisconnect);
     this.port.onMessage.addListener(this.handlePortMessage);
-    globalThis.addEventListener(EVENTS.MESSAGE, this.handleWindowMessage);
 
     this.announceAriaAlert();
   };
@@ -168,7 +156,6 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
     }
 
     this.updateElementStyles(this.iframe, { opacity: "0", height: "0px", display: "block" });
-    globalThis.removeEventListener("message", this.handleWindowMessage);
     this.unobserveIframe();
     this.port?.onMessage.removeListener(this.handlePortMessage);
     this.port?.onDisconnect.removeListener(this.handlePortDisconnect);
@@ -265,30 +252,6 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
     );
   }
 
-  /**
-   * Handles messages sent from the iframe. If the message does not have a
-   * specified handler set, it passes the message to the background script.
-   *
-   * @param event - The message event
-   */
-  private handleWindowMessage = (event: MessageEvent) => {
-    if (
-      !this.port ||
-      event.source !== this.iframe.contentWindow ||
-      !this.isFromExtensionOrigin(event.origin.toLowerCase())
-    ) {
-      return;
-    }
-
-    const message = event.data;
-    if (this.windowMessageHandlers[message.command]) {
-      this.windowMessageHandlers[message.command](message);
-      return;
-    }
-
-    this.port.postMessage(event.data);
-  };
-
   /**
    * Accepts an element and updates the styles for that element. This method
    * will also unobserve the element if it is the iframe element. This is
@@ -311,17 +274,6 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
     this.observeIframe();
   }
 
-  /**
-   * Chrome returns null for any sandboxed iframe sources.
-   * Firefox references the extension URI as its origin.
-   * Any other origin value is a security risk.
-   *
-   * @param messageOrigin - The origin of the window message
-   */
-  private isFromExtensionOrigin(messageOrigin: string): boolean {
-    return this.extensionOriginsSet.has(messageOrigin);
-  }
-
   /**
    * Handles mutations to the iframe element. The ensures that the iframe
    * element's styles are not modified by a third party source.
@@ -351,6 +303,10 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
     }
   };
 
+  private forceCloseAutofillOverlay() {
+    void sendExtensionMessage("closeAutofillOverlay", { forceClose: true });
+  }
+
   /**
    * Handles mutations to the iframe element's attributes. This ensures that
    * the iframe element's attributes are not modified by a third party source.
@@ -366,7 +322,7 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
       }
 
       if (this.foreignMutationsCount >= 10) {
-        this.port?.postMessage({ command: "forceCloseAutofillOverlay" });
+        this.forceCloseAutofillOverlay();
         break;
       }
 
@@ -421,7 +377,7 @@ class AutofillOverlayIframeService implements AutofillOverlayIframeServiceInterf
     if (this.mutationObserverIterations > 20) {
       clearTimeout(this.mutationObserverIterationsResetTimeout);
       resetCounters();
-      this.port?.postMessage({ command: "forceCloseAutofillOverlay" });
+      this.forceCloseAutofillOverlay();
 
       return true;
     }
diff --git a/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts b/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts
index 0d68b37e2f..57ea6f89d7 100644
--- a/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts
+++ b/apps/browser/src/autofill/overlay/pages/button/autofill-overlay-button.ts
@@ -46,15 +46,20 @@ class AutofillOverlayButton extends AutofillOverlayPageElement {
    * @param authStatus - The authentication status of the user
    * @param styleSheetUrl - The URL of the stylesheet to apply to the page
    * @param translations - The translations to apply to the page
-   * @private
+   * @param messageConnectorUrl - The URL of the message connector to use
    */
   private async initAutofillOverlayButton({
     authStatus,
     styleSheetUrl,
     translations,
+    messageConnectorUrl,
   }: InitAutofillOverlayButtonMessage) {
-    const linkElement = this.initOverlayPage("button", styleSheetUrl, translations);
-
+    const linkElement = await this.initOverlayPage(
+      "button",
+      styleSheetUrl,
+      translations,
+      messageConnectorUrl,
+    );
     this.buttonElement.tabIndex = -1;
     this.buttonElement.type = "button";
     this.buttonElement.classList.add("overlay-button");
@@ -63,7 +68,7 @@ class AutofillOverlayButton extends AutofillOverlayPageElement {
       this.getTranslation("toggleBitwardenVaultOverlay"),
     );
     this.buttonElement.addEventListener(EVENTS.CLICK, this.handleButtonElementClick);
-    this.postMessageToParent({ command: "getPageColorScheme" });
+    this.postMessageToConnector({ command: "getPageColorScheme" });
 
     this.updateAuthStatus(authStatus);
 
@@ -103,7 +108,7 @@ class AutofillOverlayButton extends AutofillOverlayPageElement {
    * parent window indicating that the button was clicked.
    */
   private handleButtonElementClick = () => {
-    this.postMessageToParent({ command: "overlayButtonClicked" });
+    this.postMessageToConnector({ command: "overlayButtonClicked" });
   };
 
   /**
@@ -115,7 +120,7 @@ class AutofillOverlayButton extends AutofillOverlayPageElement {
       return;
     }
 
-    this.postMessageToParent({ command: "closeAutofillOverlay" });
+    this.postMessageToConnector({ command: "closeAutofillOverlay" });
   }
 }
 
diff --git a/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts b/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts
index 4892ec4abf..4a5466ba3e 100644
--- a/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts
+++ b/apps/browser/src/autofill/overlay/pages/list/autofill-overlay-list.ts
@@ -44,6 +44,7 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
    * @param theme - The theme to use for the overlay list.
    * @param authStatus - The current authentication status.
    * @param ciphers - The ciphers to display in the overlay list.
+   * @param messageConnectorUrl - The URL of the message connector to use.
    */
   private async initAutofillOverlayList({
     translations,
@@ -51,8 +52,14 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
     theme,
     authStatus,
     ciphers,
+    messageConnectorUrl,
   }: InitAutofillOverlayListMessage) {
-    const linkElement = this.initOverlayPage("button", styleSheetUrl, translations);
+    const linkElement = await this.initOverlayPage(
+      "list",
+      styleSheetUrl,
+      translations,
+      messageConnectorUrl,
+    );
 
     const themeClass = `theme_${theme}`;
     globalThis.document.documentElement.classList.add(themeClass);
@@ -105,7 +112,7 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
    * Sends a message to the parent window to unlock the vault.
    */
   private handleUnlockButtonClick = () => {
-    this.postMessageToParent({ command: "unlockVault" });
+    this.postMessageToConnector({ command: "unlockVault" });
   };
 
   /**
@@ -169,7 +176,7 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
    * Sends a message to the parent window to add a new vault item.
    */
   private handeNewItemButtonClick = () => {
-    this.postMessageToParent({ command: "addNewVaultItem" });
+    this.postMessageToConnector({ command: "addNewVaultItem" });
   };
 
   /**
@@ -276,7 +283,7 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
   private handleFillCipherClickEvent = (cipher: OverlayCipherData) => {
     return this.useEventHandlersMemo(
       () =>
-        this.postMessageToParent({
+        this.postMessageToConnector({
           command: "fillSelectedListItem",
           overlayCipherId: cipher.id,
         }),
@@ -341,7 +348,8 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
    */
   private handleViewCipherClickEvent = (cipher: OverlayCipherData) => {
     return this.useEventHandlersMemo(
-      () => this.postMessageToParent({ command: "viewSelectedCipher", overlayCipherId: cipher.id }),
+      () =>
+        this.postMessageToConnector({ command: "viewSelectedCipher", overlayCipherId: cipher.id }),
       `${cipher.id}-view-cipher-button-click-handler`,
     );
   };
@@ -476,7 +484,7 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
       return;
     }
 
-    this.postMessageToParent({ command: "checkAutofillOverlayButtonFocused" });
+    this.postMessageToConnector({ command: "checkAutofillOverlayButtonFocused" });
   }
 
   /**
@@ -533,7 +541,7 @@ class AutofillOverlayList extends AutofillOverlayPageElement {
       }
 
       const { height } = entry.contentRect;
-      this.postMessageToParent({
+      this.postMessageToConnector({
         command: "updateAutofillOverlayListHeight",
         styles: { height: `${height}px` },
       });
diff --git a/apps/browser/src/autofill/overlay/pages/message-connector/bootstrap-autofill-overlay-message-connector.ts b/apps/browser/src/autofill/overlay/pages/message-connector/bootstrap-autofill-overlay-message-connector.ts
new file mode 100644
index 0000000000..ef1ba474b9
--- /dev/null
+++ b/apps/browser/src/autofill/overlay/pages/message-connector/bootstrap-autofill-overlay-message-connector.ts
@@ -0,0 +1,3 @@
+import { AutofillOverlayMessageConnector } from "./message-connector";
+
+(() => new AutofillOverlayMessageConnector())();
diff --git a/apps/browser/src/autofill/overlay/pages/message-connector/message-connector.html b/apps/browser/src/autofill/overlay/pages/message-connector/message-connector.html
new file mode 100644
index 0000000000..77ea7c9ae3
--- /dev/null
+++ b/apps/browser/src/autofill/overlay/pages/message-connector/message-connector.html
@@ -0,0 +1,10 @@
+<!doctype html>
+<html lang="en">
+  <head>
+    <title>Autofill overlay message connector</title>
+    <meta charset="utf-8" />
+    <meta name="viewport" content="width=device-width,initial-scale=1" />
+    <meta name="color-scheme" content="normal" />
+  </head>
+  <body></body>
+</html>
diff --git a/apps/browser/src/autofill/overlay/pages/message-connector/message-connector.ts b/apps/browser/src/autofill/overlay/pages/message-connector/message-connector.ts
new file mode 100644
index 0000000000..9f6340cd2f
--- /dev/null
+++ b/apps/browser/src/autofill/overlay/pages/message-connector/message-connector.ts
@@ -0,0 +1,46 @@
+export class AutofillOverlayMessageConnector {
+  private extensionOriginsSet: Set<string>;
+  private port: chrome.runtime.Port | null = null;
+
+  constructor() {
+    globalThis.addEventListener("message", this.handleWindowMessage);
+
+    this.extensionOriginsSet = new Set([
+      chrome.runtime.getURL("").slice(0, -1).toLowerCase(), // Remove the trailing slash and normalize the extension url to lowercase
+      "null",
+    ]);
+  }
+
+  private handleWindowMessage = (event: MessageEvent) => {
+    if (
+      event.source !== globalThis.parent ||
+      !this.isFromExtensionOrigin(event.origin.toLowerCase())
+    ) {
+      return;
+    }
+
+    const message = event.data;
+
+    if (this.port) {
+      this.port.postMessage(message);
+      return;
+    }
+
+    if (message.command !== "initAutofillOverlayPort") {
+      return;
+    }
+
+    this.port = chrome.runtime.connect({ name: message.portName });
+  };
+
+  /**
+   * Chrome returns null for any sandboxed iframe sources.
+   * Firefox references the extension URI as its origin.
+   * Any other origin value is a security risk.
+   *
+   * @param messageOrigin - The origin of the window message
+   */
+  private isFromExtensionOrigin(messageOrigin: string): boolean {
+    return this.extensionOriginsSet.has(messageOrigin);
+  }
+}
diff --git a/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.spec.ts b/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.spec.ts
index c70892cfca..ce369b6b2d 100644
--- a/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.spec.ts
+++ b/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.spec.ts
@@ -31,11 +31,12 @@ describe("AutofillOverlayPageElement", () => {
       jest.spyOn(globalThis.document, "createElement");
     });
 
-    it("initializes the button overlay page", () => {
-      const linkElement = autofillOverlayPageElement["initOverlayPage"](
+    it("initializes the button overlay page", async () => {
+      const linkElement = await autofillOverlayPageElement["initOverlayPage"](
         "button",
         "https://jest-testing-website.com",
         translations,
+        "https://jest-testing-website.com/message-connector",
       );
 
       expect(globalThis.document.documentElement.setAttribute).toHaveBeenCalledWith(
@@ -49,16 +50,16 @@ describe("AutofillOverlayPageElement", () => {
     });
   });
 
-  describe("postMessageToParent", () => {
+  describe("postMessageToConnector", () => {
     it("skips posting a message to the parent if the message origin in not set", () => {
-      autofillOverlayPageElement["postMessageToParent"]({ command: "test" });
+      autofillOverlayPageElement["postMessageToConnector"]({ command: "test" });
 
       expect(globalThis.parent.postMessage).not.toHaveBeenCalled();
     });
 
     it("posts a message to the parent", () => {
       autofillOverlayPageElement["messageOrigin"] = "https://jest-testing-website.com";
-      autofillOverlayPageElement["postMessageToParent"]({ command: "test" });
+      autofillOverlayPageElement["postMessageToConnector"]({ command: "test" });
 
       expect(globalThis.parent.postMessage).toHaveBeenCalledWith(
         { command: "test" },
diff --git a/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.ts b/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.ts
index 34f115f401..9dffd7801d 100644
--- a/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.ts
+++ b/apps/browser/src/autofill/overlay/pages/shared/autofill-overlay-page-element.ts
@@ -1,6 +1,6 @@
 import { EVENTS } from "@bitwarden/common/autofill/constants";
 
-import { RedirectFocusDirection } from "../../../utils/autofill-overlay.enum";
+import { AutofillOverlayPort, RedirectFocusDirection } from "../../../utils/autofill-overlay.enum";
 import {
   AutofillOverlayPageElementWindowMessage,
   WindowMessageHandlers,
@@ -10,6 +10,7 @@ class AutofillOverlayPageElement extends HTMLElement {
   protected shadowDom: ShadowRoot;
   protected messageOrigin: string;
   protected translations: Record<string, string>;
+  protected messageConnectorIframe: HTMLIFrameElement;
   protected windowMessageHandlers: WindowMessageHandlers;
 
   constructor() {
@@ -25,16 +26,41 @@ class AutofillOverlayPageElement extends HTMLElement {
    * @param elementName - The name of the element, e.g. "button" or "list"
    * @param styleSheetUrl - The URL of the stylesheet to apply to the page
    * @param translations - The translations to apply to the page
+   * @param messageConnectorUrl - The URL of the message connector to use
    */
-  protected initOverlayPage(
+  protected async initOverlayPage(
     elementName: "button" | "list",
     styleSheetUrl: string,
     translations: Record<string, string>,
-  ): HTMLLinkElement {
+    messageConnectorUrl: string,
+  ): Promise<HTMLLinkElement> {
     this.translations = translations;
     globalThis.document.documentElement.setAttribute("lang", this.getTranslation("locale"));
     globalThis.document.head.title = this.getTranslation(`${elementName}PageTitle`);
 
+    this.messageConnectorIframe = globalThis.document.createElement("iframe");
+    this.messageConnectorIframe.src = messageConnectorUrl;
+    this.messageConnectorIframe.style.opacity = "0";
+    this.messageConnectorIframe.style.position = "absolute";
+    this.messageConnectorIframe.style.width = "0";
+    this.messageConnectorIframe.style.height = "0";
+    this.messageConnectorIframe.style.border = "none";
+    this.messageConnectorIframe.style.pointerEvents = "none";
+    globalThis.document.body.appendChild(this.messageConnectorIframe);
+
+    await new Promise<void>((resolve) => {
+      this.messageConnectorIframe.addEventListener(EVENTS.LOAD, () => {
+        this.postMessageToConnector({
+          command: `initAutofillOverlayPort`,
+          portName:
+            elementName === "list"
+              ? AutofillOverlayPort.ListMessageConnector
+              : AutofillOverlayPort.ButtonMessageConnector,
+        });
+        resolve();
+      });
+    });
+
     this.shadowDom.innerHTML = "";
     const linkElement = globalThis.document.createElement("link");
     linkElement.setAttribute("rel", "stylesheet");
@@ -48,12 +74,12 @@ class AutofillOverlayPageElement extends HTMLElement {
    *
    * @param message - The message to post
    */
-  protected postMessageToParent(message: AutofillOverlayPageElementWindowMessage) {
+  protected postMessageToConnector(message: AutofillOverlayPageElementWindowMessage) {
     if (!this.messageOrigin) {
       return;
     }
 
-    globalThis.parent.postMessage(message, this.messageOrigin);
+    this.messageConnectorIframe.contentWindow.postMessage(message, "*");
   }
 
   /**
@@ -111,7 +137,7 @@ class AutofillOverlayPageElement extends HTMLElement {
    * Handles the window blur event.
    */
   private handleWindowBlurEvent = () => {
-    this.postMessageToParent({ command: "overlayPageBlurred" });
+    this.postMessageToConnector({ command: "overlayPageBlurred" });
   };
 
   /**
@@ -148,7 +174,7 @@ class AutofillOverlayPageElement extends HTMLElement {
    * @param direction - The direction to redirect the focus out
    */
   private redirectOverlayFocusOutMessage(direction: string) {
-    this.postMessageToParent({ command: "redirectOverlayFocusOut", direction });
+    this.postMessageToConnector({ command: "redirectOverlayFocusOut", direction });
   }
 }
 
diff --git a/apps/browser/src/autofill/spec/autofill-mocks.ts b/apps/browser/src/autofill/spec/autofill-mocks.ts
index 708489c57e..3b87591ccc 100644
--- a/apps/browser/src/autofill/spec/autofill-mocks.ts
+++ b/apps/browser/src/autofill/spec/autofill-mocks.ts
@@ -173,6 +173,7 @@ function createInitAutofillOverlayButtonMessageMock(
     translations: overlayPagesTranslations,
     styleSheetUrl: "https://jest-testing-website.com",
     authStatus: AuthenticationStatus.Unlocked,
+    messageConnectorUrl: "https://jest-testing-website.com/message-connector",
     ...customFields,
   };
 }
@@ -203,6 +204,7 @@ function createInitAutofillOverlayListMessageMock(
     styleSheetUrl: "https://jest-testing-website.com",
     theme: ThemeType.Light,
     authStatus: AuthenticationStatus.Unlocked,
+    messageConnectorUrl: "https://jest-testing-website.com/message-connector",
     ciphers: [
       createAutofillOverlayCipherDataMock(1, {
         icon: {
diff --git a/apps/browser/src/autofill/utils/autofill-overlay.enum.ts b/apps/browser/src/autofill/utils/autofill-overlay.enum.ts
index 486d68f754..ed2030324d 100644
--- a/apps/browser/src/autofill/utils/autofill-overlay.enum.ts
+++ b/apps/browser/src/autofill/utils/autofill-overlay.enum.ts
@@ -5,7 +5,9 @@ const AutofillOverlayElement = {
 
 const AutofillOverlayPort = {
   Button: "autofill-overlay-button-port",
+  ButtonMessageConnector: "autofill-overlay-button-message-connector",
   List: "autofill-overlay-list-port",
+  ListMessageConnector: "autofill-overlay-list-message-connector",
 } as const;
 
 const RedirectFocusDirection = {
diff --git a/apps/browser/src/manifest.json b/apps/browser/src/manifest.json
index d1979b4e23..89421309b7 100644
--- a/apps/browser/src/manifest.json
+++ b/apps/browser/src/manifest.json
@@ -115,6 +115,7 @@
     "images/icon38_locked.png",
     "overlay/button.html",
     "overlay/list.html",
+    "overlay/message-connector.html",
     "popup/fonts/*"
   ],
   "applications": {
diff --git a/apps/browser/src/manifest.v3.json b/apps/browser/src/manifest.v3.json
index e7b0c0cd1e..23a0e06c4d 100644
--- a/apps/browser/src/manifest.v3.json
+++ b/apps/browser/src/manifest.v3.json
@@ -119,6 +119,7 @@
         "images/icon38_locked.png",
         "overlay/button.html",
         "overlay/list.html",
+        "overlay/message-connector.html",
         "popup/fonts/*"
       ],
       "matches": ["<all_urls>"]
diff --git a/apps/browser/webpack.config.js b/apps/browser/webpack.config.js
index 3b5724b198..82d12086a4 100644
--- a/apps/browser/webpack.config.js
+++ b/apps/browser/webpack.config.js
@@ -116,6 +116,11 @@ const plugins = [
     filename: "overlay/list.html",
     chunks: ["overlay/list"],
   }),
+  new HtmlWebpackPlugin({
+    template: "./src/autofill/overlay/pages/message-connector/message-connector.html",
+    filename: "overlay/message-connector.html",
+    chunks: ["overlay/message-connector"],
+  }),
   new CopyWebpackPlugin({
     patterns: [
       manifestVersion == 3
@@ -173,6 +178,8 @@ const mainConfig = {
     "notification/bar": "./src/autofill/notification/bar.ts",
     "overlay/button": "./src/autofill/overlay/pages/button/bootstrap-autofill-overlay-button.ts",
     "overlay/list": "./src/autofill/overlay/pages/list/bootstrap-autofill-overlay-list.ts",
+    "overlay/message-connector":
+      "./src/autofill/overlay/pages/message-connector/bootstrap-autofill-overlay-message-connector.ts",
     "encrypt-worker": "../../libs/common/src/platform/services/cryptography/encrypt.worker.ts",
     "content/lp-fileless-importer": "./src/tools/content/lp-fileless-importer.ts",
     "content/send-on-installed-message": "./src/vault/content/send-on-installed-message.ts",