diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 719e5603ad5..419f6faa615 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -343,15 +343,33 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       await this.buildSubFrameOffsets(sender.tab, frameId, sender.url);
     }
 
-    this.updateInlineMenuPositionTimeout = setTimeout(() => {
-      if (this.isFieldCurrentlyFocused) {
-        void this.updateInlineMenuPosition({ overlayElement: AutofillOverlayElement.List }, sender);
-        void this.updateInlineMenuPosition(
-          { overlayElement: AutofillOverlayElement.Button },
-          sender,
-        );
-      }
-    }, 650);
+    this.updateInlineMenuPositionTimeout = setTimeout(
+      () => this.updateInlineMenuPositionAfterSubFrameRebuild(sender),
+      650,
+    );
+  }
+
+  private async updateInlineMenuPositionAfterSubFrameRebuild(sender: chrome.runtime.MessageSender) {
+    if (!this.isFieldCurrentlyFocused) {
+      return;
+    }
+
+    void this.updateInlineMenuPosition({ overlayElement: AutofillOverlayElement.Button }, sender);
+
+    const mostRecentlyFocusedFieldHasValue = await BrowserApi.tabSendMessage(
+      sender.tab,
+      { command: "checkMostRecentlyFocusedFieldHasValue" },
+      { frameId: this.focusedFieldData.frameId },
+    );
+    if (
+      mostRecentlyFocusedFieldHasValue &&
+      (this.checkIsOverlayLoginCiphersPopulated(sender) ||
+        this.userAuthStatus !== AuthenticationStatus.Unlocked)
+    ) {
+      return;
+    }
+
+    void this.updateInlineMenuPosition({ overlayElement: AutofillOverlayElement.List }, sender);
   }
 
   /**
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 ce5f1a24487..36575a6d73e 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
@@ -23,6 +23,7 @@ export type AutofillOverlayContentExtensionMessageHandlers = {
   updateAutofillInlineMenuVisibility: ({ message }: AutofillExtensionMessageParam) => void;
   getSubFrameOffsets: ({ message }: AutofillExtensionMessageParam) => Promise<SubFrameOffsetData>;
   getSubFrameOffsetsFromWindowMessage: ({ message }: AutofillExtensionMessageParam) => void;
+  checkMostRecentlyFocusedFieldHasValue: () => boolean;
 };
 
 export interface AutofillOverlayContentService {
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 b65dcd3cd1f..00688e4c175 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -54,6 +54,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     getSubFrameOffsets: ({ message }) => this.getSubFrameOffsets(message),
     getSubFrameOffsetsFromWindowMessage: ({ message }) =>
       this.getSubFrameOffsetsFromWindowMessage(message),
+    checkMostRecentlyFocusedFieldHasValue: () => this.mostRecentlyFocusedFieldHasValue(),
   };
 
   /**
@@ -859,6 +860,10 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     );
   }
 
+  private mostRecentlyFocusedFieldHasValue() {
+    return Boolean((this.mostRecentlyFocusedField as FillableFormFieldElement)?.value);
+  }
+
   /**
    * Sets up global event listeners and the mutation
    * observer to facilitate required changes to the