diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 68d3f32b80..db50b78445 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -216,6 +216,7 @@ export type OverlayBackgroundExtensionMessageHandlers = {
   getCurrentTabFrameId: ({ sender }: BackgroundSenderParam) => number;
   updateSubFrameData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   triggerSubFrameFocusInRebuild: ({ sender }: BackgroundSenderParam) => void;
+  shouldRepositionSubFrameInlineMenuOnScroll: ({ sender }: BackgroundSenderParam) => void;
   destroyAutofillInlineMenuListeners: ({
     message,
     sender,
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 2b8f2c273c..dd549cddbf 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -168,6 +168,8 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     getCurrentTabFrameId: ({ sender }) => this.getSenderFrameId(sender),
     updateSubFrameData: ({ message, sender }) => this.updateSubFrameData(message, sender),
     triggerSubFrameFocusInRebuild: ({ sender }) => this.triggerSubFrameFocusInRebuild(sender),
+    shouldRepositionSubFrameInlineMenuOnScroll: ({ sender }) =>
+      this.shouldRepositionSubFrameInlineMenuOnScroll(sender),
     destroyAutofillInlineMenuListeners: ({ message, sender }) =>
       this.triggerDestroyInlineMenuListeners(sender.tab, message.subFrameData.frameId),
     collectPageDetailsResponse: ({ message, sender }) => this.storePageDetails(message, sender),
@@ -2594,6 +2596,14 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     this.repositionInlineMenu$.next(sender);
   }
 
+  private shouldRepositionSubFrameInlineMenuOnScroll(sender: chrome.runtime.MessageSender) {
+    if (!this.isFieldCurrentlyFocused || sender.tab.id !== this.focusedFieldData?.tabId) {
+      return false;
+    }
+
+    return this.focusedFieldData.frameId > 0;
+  }
+
   /**
    * Handles determining if the inline menu should be repositioned or closed, and initiates
    * the process of calculating the new position of 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 760a585bd6..645795d9f2 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -1571,14 +1571,35 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       AUTOFILL_OVERLAY_HANDLE_REPOSITION,
     );
 
-    const eventTargetDoesNotContainFocusedField = (element: Element) =>
-      typeof element?.contains === "function" && !element.contains(this.mostRecentlyFocusedField);
+    const eventTargetContainsFocusedField = (eventTarget: Element | Document) => {
+      if (!eventTarget || !this.mostRecentlyFocusedField) {
+        return false;
+      }
+
+      const activeElement = (eventTarget as Document).activeElement;
+      if (activeElement) {
+        return (
+          activeElement === this.mostRecentlyFocusedField ||
+          activeElement.contains(this.mostRecentlyFocusedField)
+        );
+      }
+
+      if (typeof eventTarget.contains !== "function") {
+        return false;
+      }
+      return (
+        eventTarget === this.mostRecentlyFocusedField ||
+        eventTarget.contains(this.mostRecentlyFocusedField)
+      );
+    };
     const scrollHandler = this.useEventHandlersMemo(
-      throttle((event) => {
-        if (eventTargetDoesNotContainFocusedField(event.target as Element)) {
-          return;
+      throttle(async (event) => {
+        if (
+          eventTargetContainsFocusedField(event.target) ||
+          (await this.shouldRepositionSubFrameInlineMenuOnScroll())
+        ) {
+          repositionHandler(event);
         }
-        repositionHandler(event);
       }, 50),
       AUTOFILL_OVERLAY_HANDLE_SCROLL,
     );
@@ -1590,6 +1611,10 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     globalThis.addEventListener(EVENTS.RESIZE, repositionHandler);
   }
 
+  private shouldRepositionSubFrameInlineMenuOnScroll = async () => {
+    return await this.sendExtensionMessage("shouldRepositionSubFrameInlineMenuOnScroll");
+  };
+
   /**
    * Removes the listeners that facilitate repositioning
    * the overlay elements on scroll or resize.