diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 8ea643cf60c..ae233de7509 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -112,6 +112,7 @@ type OverlayBackgroundExtensionMessageHandlers = {
   updateIsFieldCurrentlyFilling: ({ message }: BackgroundMessageParam) => void;
   checkIsInlineMenuButtonVisible: ({ sender }: BackgroundSenderParam) => void;
   checkIsInlineMenuListVisible: ({ sender }: BackgroundSenderParam) => void;
+  checkIsInlineMenuCiphersPopulated: ({ sender }: BackgroundSenderParam) => void;
   updateSubFrameData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   rebuildSubFrameOffsets: ({ sender }: BackgroundSenderParam) => void;
 };
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 46803af7d45..bba50cce27b 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -85,6 +85,8 @@ class OverlayBackground implements OverlayBackgroundInterface {
       (this.isCurrentlyFilling = message.isFieldCurrentlyFilling),
     checkIsInlineMenuButtonVisible: ({ sender }) => this.checkIsInlineMenuButtonVisible(sender),
     checkIsInlineMenuListVisible: ({ sender }) => this.checkIsInlineMenuListVisible(sender),
+    checkIsInlineMenuCiphersPopulated: ({ sender }) =>
+      this.checkIsInlineMenuCiphersPopulated(sender),
     updateSubFrameData: ({ message, sender }) => this.updateSubFrameData(message, sender),
     rebuildSubFrameOffsets: ({ sender }) => this.rebuildSubFrameOffsets(sender),
   };
@@ -137,6 +139,10 @@ class OverlayBackground implements OverlayBackgroundInterface {
     );
   }
 
+  private checkIsInlineMenuCiphersPopulated(sender: chrome.runtime.MessageSender) {
+    return sender.tab.id === this.focusedFieldData.tabId && this.overlayLoginCiphers.size > 0;
+  }
+
   updateSubFrameData(message: any, sender: chrome.runtime.MessageSender) {
     const subFrameOffsetsForTab = this.subFrameOffsetsForTab[sender.tab.id];
     if (subFrameOffsetsForTab) {
@@ -199,9 +205,6 @@ class OverlayBackground implements OverlayBackgroundInterface {
 
     const ciphers = await this.getOverlayCipherData();
     this.overlayListPort?.postMessage({ command: "updateOverlayListCiphers", ciphers });
-    await BrowserApi.tabSendMessageData(currentTab, "updateIsOverlayCiphersPopulated", {
-      isOverlayCiphersPopulated: Boolean(ciphers.length),
-    });
   }
 
   /**
diff --git a/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts b/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts
index 21bd964ee42..0256c9b0c19 100644
--- a/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/abstractions/autofill-overlay-content.service.ts
@@ -20,15 +20,11 @@ export type AutofillOverlayContentExtensionMessageHandlers = {
   bgVaultItemRepromptPopoutOpened: () => void;
   redirectOverlayFocusOut: ({ message }: AutofillExtensionMessageParam) => void;
   updateAutofillOverlayVisibility: ({ message }: AutofillExtensionMessageParam) => void;
-  updateIsOverlayCiphersPopulated: ({ message }: AutofillExtensionMessageParam) => void;
   getSubFrameOffsets: ({ message }: AutofillExtensionMessageParam) => Promise<SubFrameOffsetData>;
   getSubFrameOffsetsFromWindowMessage: ({ message }: AutofillExtensionMessageParam) => void;
 };
 
 export interface AutofillOverlayContentService {
-  // isFieldCurrentlyFocused: boolean;
-  // isCurrentlyFilling: boolean;
-  isOverlayCiphersPopulated: boolean;
   pageDetailsUpdateRequired: boolean;
   autofillOverlayVisibility: number;
   extensionMessageHandlers: any;
@@ -37,11 +33,6 @@ export interface AutofillOverlayContentService {
     autofillFieldElement: ElementWithOpId<FormFieldElement>,
     autofillFieldData: AutofillField,
   ): Promise<void>;
-  openAutofillOverlay(options: OpenAutofillOverlayOptions): void;
-  // removeAutofillOverlay(): void;
-  // removeAutofillOverlayButton(): void;
-  // removeAutofillOverlayList(): void;
-  addNewVaultItem(): void;
   focusMostRecentOverlayField(): void;
   blurMostRecentOverlayField(isRemovingOverlay?: boolean): void;
   destroy(): void;
diff --git a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
index 27c3033cbd2..7a15f74ced1 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -23,7 +23,6 @@ import {
 import { AutoFillConstants } from "./autofill-constants";
 
 class AutofillOverlayContentService implements AutofillOverlayContentServiceInterface {
-  isOverlayCiphersPopulated = false;
   pageDetailsUpdateRequired = false;
   autofillOverlayVisibility: number;
   private readonly findTabs = tabbable;
@@ -47,7 +46,6 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
     bgVaultItemRepromptPopoutOpened: () => this.blurMostRecentOverlayField(true),
     redirectOverlayFocusOut: ({ message }) => this.redirectOverlayFocusOut(message),
     updateAutofillOverlayVisibility: ({ message }) => this.updateAutofillOverlayVisibility(message),
-    updateIsOverlayCiphersPopulated: ({ message }) => this.updateIsOverlayCiphersPopulated(message),
     getSubFrameOffsets: ({ message }) => this.getSubFrameOffsets(message),
     getSubFrameOffsetsFromWindowMessage: ({ message }) =>
       this.getSubFrameOffsetsFromWindowMessage(message),
@@ -365,14 +363,17 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
    *
    * @param formFieldElement - The form field element that triggered the input event.
    */
-  private triggerFormFieldInput(formFieldElement: ElementWithOpId<FormFieldElement>) {
+  private async triggerFormFieldInput(formFieldElement: ElementWithOpId<FormFieldElement>) {
     if (!elementIsFillableFormField(formFieldElement)) {
       return;
     }
 
     this.storeModifiedFormElement(formFieldElement);
 
-    if (formFieldElement.value && (this.isOverlayCiphersPopulated || !this.isUserAuthed())) {
+    if (
+      formFieldElement.value &&
+      ((await this.isOverlayCiphersPopulated()) || !this.isUserAuthed())
+    ) {
       void this.sendExtensionMessage("closeAutofillOverlay", {
         overlayElement: AutofillOverlayElement.List,
         forceCloseOverlay: true,
@@ -475,7 +476,10 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
       });
     }
 
-    if (!formElementHasValue || (!this.isOverlayCiphersPopulated && this.isUserAuthed())) {
+    if (
+      !formElementHasValue ||
+      (!(await this.isOverlayCiphersPopulated()) && this.isUserAuthed())
+    ) {
       void this.sendExtensionMessage("openAutofillOverlay");
       return;
     }
@@ -764,9 +768,12 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
 
     await this.updateMostRecentlyFocusedField(this.mostRecentlyFocusedField);
     this.updateOverlayElementsPosition();
-    setTimeout(() => {
+    setTimeout(async () => {
       this.toggleOverlayHidden(false);
-      if ((this.mostRecentlyFocusedField as HTMLInputElement).value) {
+      if (
+        (this.mostRecentlyFocusedField as HTMLInputElement).value &&
+        ((await this.isOverlayCiphersPopulated()) || !this.isUserAuthed())
+      ) {
         void this.sendExtensionMessage("closeAutofillOverlay", {
           overlayElement: AutofillOverlayElement.List,
           forceCloseOverlay: true,
@@ -946,8 +953,8 @@ class AutofillOverlayContentService implements AutofillOverlayContentServiceInte
     this.autofillOverlayVisibility = data.autofillOverlayVisibility;
   }
 
-  private updateIsOverlayCiphersPopulated({ data }: AutofillExtensionMessage) {
-    this.isOverlayCiphersPopulated = Boolean(data?.isOverlayCiphersPopulated);
+  private async isOverlayCiphersPopulated() {
+    return (await this.sendExtensionMessage("checkIsInlineMenuCiphersPopulated")) === true;
   }
 
   /**