diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 7887658a9a..70151719d4 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -12,10 +12,11 @@ export type PageDetailsForTab = Record<
 >;
 
 export type SubFrameOffsetData = {
-  frameId?: number;
-  url?: string;
   top: number;
   left: number;
+  url?: string;
+  frameId?: number;
+  parentFrameIds?: number[];
 } | null;
 
 export type SubFrameOffsetsForTab = Record<
@@ -116,6 +117,8 @@ export type OverlayBackgroundExtensionMessageHandlers = {
   updateAutofillInlineMenuHidden: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   checkIsAutofillInlineMenuButtonVisible: ({ sender }: BackgroundSenderParam) => void;
   checkIsAutofillInlineMenuListVisible: ({ sender }: BackgroundSenderParam) => void;
+  checkShouldRepositionInlineMenu: ({ sender }: BackgroundSenderParam) => boolean;
+  getCurrentTabFrameId: ({ sender }: BackgroundSenderParam) => number;
   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 05eff398ba..7b124da1e1 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -88,6 +88,8 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       this.checkIsAutofillInlineMenuButtonVisible(sender),
     checkIsAutofillInlineMenuListVisible: ({ sender }) =>
       this.checkIsAutofillInlineMenuListVisible(sender),
+    checkShouldRepositionInlineMenu: ({ sender }) => this.checkShouldRepositionInlineMenu(sender),
+    getCurrentTabFrameId: ({ sender }) => this.getCurrentFrameId(sender),
     updateSubFrameData: ({ message, sender }) => this.updateSubFrameData(message, sender),
     rebuildSubFrameOffsets: ({ sender }) => this.rebuildSubFrameOffsets(sender),
     collectPageDetailsResponse: ({ message, sender }) => this.storePageDetails(message, sender),
@@ -256,6 +258,10 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     pageDetailsMap.set(sender.frameId, pageDetails);
   }
 
+  private getCurrentFrameId(sender: chrome.runtime.MessageSender) {
+    return sender.frameId;
+  }
+
   /**
    * Handles sub frame offset calculations for the given tab and frame id.
    * Is used in setting the position of the inline menu list and button.
@@ -293,7 +299,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       return;
     }
 
-    const subFrameData = { url, top: 0, left: 0 };
+    const subFrameData: SubFrameOffsetData = { url, top: 0, left: 0, parentFrameIds: [] };
     let frameDetails = await BrowserApi.getFrameDetails({ tabId, frameId });
 
     while (frameDetails && frameDetails.parentFrameId > -1) {
@@ -319,6 +325,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
 
       subFrameData.top += subFrameOffset.top;
       subFrameData.left += subFrameOffset.left;
+      subFrameData.parentFrameIds.push(frameDetails.parentFrameId);
 
       frameDetails = await BrowserApi.getFrameDetails({
         tabId,
@@ -1005,6 +1012,34 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     );
   }
 
+  private checkShouldRepositionInlineMenu(sender: chrome.runtime.MessageSender): boolean {
+    if (
+      !this.focusedFieldData ||
+      sender.tab.id !== this.focusedFieldData.tabId ||
+      !this.isFieldCurrentlyFocused
+    ) {
+      return false;
+    }
+
+    if (this.focusedFieldData.frameId === sender.frameId) {
+      return true;
+    }
+
+    const subFrameOffsetsForTab = this.subFrameOffsetsForTab[sender.tab.id];
+    if (!subFrameOffsetsForTab) {
+      return false;
+    }
+
+    const parentFrameIds = new Set();
+    subFrameOffsetsForTab.forEach((subFrameOffsetData) =>
+      subFrameOffsetData.parentFrameIds.forEach((parentFrameId) =>
+        parentFrameIds.add(parentFrameId),
+      ),
+    );
+
+    return parentFrameIds.has(sender.frameId);
+  }
+
   /**
    * Responds to the content script's request to check if the inline menu ciphers are populated.
    * This will return true only if the sender is the focused field's tab and the inline menu
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 d23faf3fab..d265d84652 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -765,17 +765,18 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     globalThis.removeEventListener(EVENTS.RESIZE, this.handleOverlayRepositionEvent);
   }
 
+  private overlayRepositionTimeout: number | NodeJS.Timeout;
+
   /**
    * Handles the resize or scroll events that enact
    * repositioning of existing overlay elements.
    */
   private handleOverlayRepositionEvent = async () => {
-    this.rebuildSubFrameOffsets();
-
-    if (!(await this.isInlineMenuButtonVisible()) && !(await this.isInlineMenuListVisible())) {
+    if (!(await this.sendExtensionMessage("checkShouldRepositionInlineMenu"))) {
       return;
     }
 
+    this.rebuildSubFrameOffsets();
     this.toggleAutofillInlineMenuHidden(true);
     this.clearUserInteractionEventTimeout();
     this.userInteractionEventTimeout = setTimeout(this.triggerOverlayRepositionUpdates, 750);
@@ -957,6 +958,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
           frameId: message.subFrameId,
           left: 0,
           top: 0,
+          parentFrameIds: [],
         },
       },
       "*",
@@ -968,10 +970,10 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       return;
     }
 
-    this.calculateSubFramePositioning(event);
+    void this.calculateSubFramePositioning(event);
   };
 
-  private calculateSubFramePositioning = (event: MessageEvent) => {
+  private calculateSubFramePositioning = async (event: MessageEvent) => {
     const subFrameData = event.data.subFrameData;
     let subFrameOffsets: SubFrameOffsetData;
     const iframes = document.querySelectorAll("iframe");
@@ -983,9 +985,11 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
           subFrameData.url,
           subFrameData.frameId,
         );
+        const parentFrameId = await this.sendExtensionMessage("getCurrentTabFrameId");
 
         subFrameData.top += subFrameOffsets.top;
         subFrameData.left += subFrameOffsets.left;
+        subFrameData.parentFrameIds.push(parentFrameId);
 
         break;
       }