diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 947307a7537..2df72e2f4b3 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -92,11 +92,17 @@ export type BackgroundOnMessageHandlerParams = BackgroundMessageParam & Backgrou
 
 export type OverlayBackgroundExtensionMessageHandlers = {
   [key: string]: CallableFunction;
-  openAutofillInlineMenu: () => void;
-  closeAutofillInlineMenu: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   autofillOverlayElementClosed: ({ message }: BackgroundMessageParam) => void;
   autofillOverlayAddNewVaultItem: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
+  checkIsOverlayLoginCiphersPopulated: ({ sender }: BackgroundSenderParam) => void;
+  updateFocusedFieldData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
+  updateIsFieldCurrentlyFocused: ({ message }: BackgroundMessageParam) => void;
+  checkIsFieldCurrentlyFocused: () => boolean;
+  updateIsFieldCurrentlyFilling: ({ message }: BackgroundMessageParam) => void;
+  checkIsFieldCurrentlyFilling: () => boolean;
   getAutofillInlineMenuVisibility: () => void;
+  openAutofillInlineMenu: () => void;
+  closeAutofillInlineMenu: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   checkAutofillInlineMenuFocused: () => void;
   focusAutofillInlineMenuList: () => void;
   updateAutofillInlineMenuPosition: ({
@@ -104,14 +110,8 @@ export type OverlayBackgroundExtensionMessageHandlers = {
     sender,
   }: BackgroundOnMessageHandlerParams) => Promise<void>;
   updateAutofillInlineMenuHidden: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
-  updateFocusedFieldData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
-  updateIsFieldCurrentlyFocused: ({ message }: BackgroundMessageParam) => void;
-  checkIsFieldCurrentlyFocused: () => boolean;
-  updateIsFieldCurrentlyFilling: ({ message }: BackgroundMessageParam) => void;
-  checkIsFieldCurrentlyFilling: () => boolean;
   checkIsAutofillInlineMenuButtonVisible: ({ sender }: BackgroundSenderParam) => void;
   checkIsAutofillInlineMenuListVisible: ({ sender }: BackgroundSenderParam) => void;
-  checkIsOverlayLoginCiphersPopulated: ({ sender }: BackgroundSenderParam) => void;
   updateSubFrameData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   rebuildSubFrameOffsets: ({ sender }: BackgroundSenderParam) => void;
   collectPageDetailsResponse: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index b0ee30a7662..a0ffc446eec 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -64,28 +64,28 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   private inlineMenuPageTranslations: Record<string, string>;
   private iconsServerUrl: string;
   private readonly extensionMessageHandlers: OverlayBackgroundExtensionMessageHandlers = {
-    openAutofillInlineMenu: () => this.openInlineMenu(false),
-    closeAutofillInlineMenu: ({ message, sender }) => this.closeInlineMenu(sender, message),
     autofillOverlayElementClosed: ({ message }) => this.overlayElementClosed(message),
     autofillOverlayAddNewVaultItem: ({ message, sender }) => this.addNewVaultItem(message, sender),
+    checkIsOverlayLoginCiphersPopulated: ({ sender }) =>
+      this.checkIsOverlayLoginCiphersPopulated(sender),
+    updateFocusedFieldData: ({ message, sender }) => this.setFocusedFieldData(message, sender),
+    updateIsFieldCurrentlyFocused: ({ message }) => this.updateIsFieldCurrentlyFocused(message),
+    checkIsFieldCurrentlyFocused: () => this.checkIsFieldCurrentlyFocused(),
+    updateIsFieldCurrentlyFilling: ({ message }) => this.updateIsFieldCurrentlyFilling(message),
+    checkIsFieldCurrentlyFilling: () => this.checkIsFieldCurrentlyFilling(),
     getAutofillInlineMenuVisibility: () => this.getInlineMenuVisibility(),
+    openAutofillInlineMenu: () => this.openInlineMenu(false),
+    closeAutofillInlineMenu: ({ message, sender }) => this.closeInlineMenu(sender, message),
     checkAutofillInlineMenuFocused: () => this.checkInlineMenuFocused(),
     focusAutofillInlineMenuList: () => this.focusInlineMenuList(),
     updateAutofillInlineMenuPosition: ({ message, sender }) =>
       this.updateInlineMenuPosition(message, sender),
     updateAutofillInlineMenuHidden: ({ message, sender }) =>
       this.updateInlineMenuHidden(message, sender),
-    updateFocusedFieldData: ({ message, sender }) => this.setFocusedFieldData(message, sender),
-    updateIsFieldCurrentlyFocused: ({ message }) => this.updateIsFieldCurrentlyFocused(message),
-    checkIsFieldCurrentlyFocused: () => this.checkIsFieldCurrentlyFocused(),
-    updateIsFieldCurrentlyFilling: ({ message }) => this.updateIsFieldCurrentlyFilling(message),
-    checkIsFieldCurrentlyFilling: () => this.checkIsFieldCurrentlyFilling(),
     checkIsAutofillInlineMenuButtonVisible: ({ sender }) =>
       this.checkIsAutofillInlineMenuButtonVisible(sender),
     checkIsAutofillInlineMenuListVisible: ({ sender }) =>
       this.checkIsAutofillInlineMenuListVisible(sender),
-    checkIsOverlayLoginCiphersPopulated: ({ sender }) =>
-      this.checkIsOverlayLoginCiphersPopulated(sender),
     updateSubFrameData: ({ message, sender }) => this.updateSubFrameData(message, sender),
     rebuildSubFrameOffsets: ({ sender }) => this.rebuildSubFrameOffsets(sender),
     collectPageDetailsResponse: ({ message, sender }) => this.storePageDetails(message, sender),
diff --git a/apps/browser/src/autofill/content/autofill-init.ts b/apps/browser/src/autofill/content/autofill-init.ts
index 6d23b7b55ae..d28af1f65fd 100644
--- a/apps/browser/src/autofill/content/autofill-init.ts
+++ b/apps/browser/src/autofill/content/autofill-init.ts
@@ -40,21 +40,7 @@ class AutofillInit implements AutofillInitInterface {
     inlineMenuElements?: AutofillInlineMenuContentService,
   ) {
     this.autofillOverlayContentService = autofillOverlayContentService;
-    if (this.autofillOverlayContentService) {
-      this.extensionMessageHandlers = Object.assign(
-        this.extensionMessageHandlers,
-        this.autofillOverlayContentService.extensionMessageHandlers,
-      );
-    }
-
     this.autofillInlineMenuContentService = inlineMenuElements;
-    if (this.autofillInlineMenuContentService) {
-      this.extensionMessageHandlers = Object.assign(
-        this.extensionMessageHandlers,
-        this.autofillInlineMenuContentService.extensionMessageHandlers,
-      );
-    }
-
     this.domElementVisibilityService = new DomElementVisibilityService(
       this.autofillInlineMenuContentService,
     );
@@ -190,7 +176,7 @@ class AutofillInit implements AutofillInitInterface {
     sendResponse: (response?: any) => void,
   ): boolean => {
     const command: string = message.command;
-    const handler: CallableFunction | undefined = this.extensionMessageHandlers[command];
+    const handler: CallableFunction | undefined = this.getExtensionMessageHandler(command);
     if (!handler) {
       return;
     }
@@ -204,6 +190,18 @@ class AutofillInit implements AutofillInitInterface {
     return true;
   };
 
+  private getExtensionMessageHandler(command: string): CallableFunction | undefined {
+    if (this.autofillOverlayContentService?.extensionMessageHandlers?.[command]) {
+      return this.autofillOverlayContentService.extensionMessageHandlers[command];
+    }
+
+    if (this.autofillInlineMenuContentService?.extensionMessageHandlers?.[command]) {
+      return this.autofillInlineMenuContentService.extensionMessageHandlers[command];
+    }
+
+    return this.extensionMessageHandlers[command];
+  }
+
   /**
    * Handles destroying the autofill init content script. Removes all
    * listeners, timeouts, and object instances to prevent memory leaks.