diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 401196b256..57eb391e4d 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -161,7 +161,7 @@ export type OverlayBackgroundExtensionMessageHandlers = {
   triggerAutofillOverlayReposition: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   checkIsInlineMenuCiphersPopulated: ({ sender }: BackgroundSenderParam) => void;
   updateFocusedFieldData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
-  updateIsFieldCurrentlyFocused: ({ message }: BackgroundMessageParam) => void;
+  updateIsFieldCurrentlyFocused: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   checkIsFieldCurrentlyFocused: () => boolean;
   updateIsFieldCurrentlyFilling: ({ message }: BackgroundMessageParam) => void;
   checkIsFieldCurrentlyFilling: () => boolean;
diff --git a/apps/browser/src/autofill/background/overlay.background.spec.ts b/apps/browser/src/autofill/background/overlay.background.spec.ts
index 783010ee04..725c91510d 100644
--- a/apps/browser/src/autofill/background/overlay.background.spec.ts
+++ b/apps/browser/src/autofill/background/overlay.background.spec.ts
@@ -526,10 +526,13 @@ describe("OverlayBackground", () => {
           });
 
           it("skips updating the position of either inline menu element if a field is not currently focused", async () => {
-            sendMockExtensionMessage({
-              command: "updateIsFieldCurrentlyFocused",
-              isFieldCurrentlyFocused: false,
-            });
+            sendMockExtensionMessage(
+              {
+                command: "updateIsFieldCurrentlyFocused",
+                isFieldCurrentlyFocused: false,
+              },
+              mock<chrome.runtime.MessageSender>({ frameId: 20 }),
+            );
 
             sendMockExtensionMessage({ command: "triggerAutofillOverlayReposition" }, sender);
             await flushUpdateInlineMenuPromises();
@@ -1362,6 +1365,25 @@ describe("OverlayBackground", () => {
       });
     });
 
+    describe("updateIsFieldCurrentlyFocused message handler", () => {
+      it("skips updating the isFiledCurrentlyFocused value when the focused field data is populated and the sender frame id does not equal the focused field's frame id", async () => {
+        const focusedFieldData = createFocusedFieldDataMock();
+        sendMockExtensionMessage(
+          { command: "updateFocusedFieldData", focusedFieldData },
+          mock<chrome.runtime.MessageSender>({ tab: { id: 1 }, frameId: 10 }),
+        );
+        overlayBackground["isFieldCurrentlyFocused"] = true;
+
+        sendMockExtensionMessage(
+          { command: "updateIsFieldCurrentlyFocused", isFieldCurrentlyFocused: false },
+          mock<chrome.runtime.MessageSender>({ tab: { id: 1 }, frameId: 20 }),
+        );
+        await flushPromises();
+
+        expect(overlayBackground["isFieldCurrentlyFocused"]).toBe(true);
+      });
+    });
+
     describe("checkIsFieldCurrentlyFocused message handler", () => {
       it("returns true when a form field is currently focused", async () => {
         sendMockExtensionMessage({
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 029d2d69ac..ed70a14c4a 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -97,7 +97,8 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     checkIsInlineMenuCiphersPopulated: ({ sender }) =>
       this.checkIsInlineMenuCiphersPopulated(sender),
     updateFocusedFieldData: ({ message, sender }) => this.setFocusedFieldData(message, sender),
-    updateIsFieldCurrentlyFocused: ({ message }) => this.updateIsFieldCurrentlyFocused(message),
+    updateIsFieldCurrentlyFocused: ({ message, sender }) =>
+      this.updateIsFieldCurrentlyFocused(message, sender),
     checkIsFieldCurrentlyFocused: () => this.checkIsFieldCurrentlyFocused(),
     updateIsFieldCurrentlyFilling: ({ message }) => this.updateIsFieldCurrentlyFilling(message),
     checkIsFieldCurrentlyFilling: () => this.checkIsFieldCurrentlyFilling(),
@@ -1090,7 +1091,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     { focusedFieldData }: OverlayBackgroundExtensionMessage,
     sender: chrome.runtime.MessageSender,
   ) {
-    if (this.focusedFieldData?.frameId && this.focusedFieldData.frameId !== sender.frameId) {
+    if (this.focusedFieldData && !this.senderFrameHasFocusedField(sender)) {
       void BrowserApi.tabSendMessage(
         sender.tab,
         { command: "unsetMostRecentlyFocusedField" },
@@ -1100,6 +1101,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
 
     const previousFocusedFieldData = this.focusedFieldData;
     this.focusedFieldData = { ...focusedFieldData, tabId: sender.tab.id, frameId: sender.frameId };
+    this.isFieldCurrentlyFocused = true;
 
     const accountCreationFieldBlurred =
       previousFocusedFieldData?.showInlineMenuAccountCreation &&
@@ -1558,8 +1560,16 @@ export class OverlayBackground implements OverlayBackgroundInterface {
    * Updates the property that identifies if a form field set up for the inline menu is currently focused.
    *
    * @param message - The message received from the web page
+   * @param sender - The sender of the port message
    */
-  private updateIsFieldCurrentlyFocused(message: OverlayBackgroundExtensionMessage) {
+  private updateIsFieldCurrentlyFocused(
+    message: OverlayBackgroundExtensionMessage,
+    sender: chrome.runtime.MessageSender,
+  ) {
+    if (this.focusedFieldData && !this.senderFrameHasFocusedField(sender)) {
+      return;
+    }
+
     this.isFieldCurrentlyFocused = message.isFieldCurrentlyFocused;
   }
 
@@ -1651,7 +1661,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       return false;
     }
 
-    if (this.focusedFieldData?.frameId === sender.frameId) {
+    if (this.senderFrameHasFocusedField(sender)) {
       return true;
     }
 
@@ -1676,6 +1686,15 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     return sender.tab.id === this.focusedFieldData?.tabId;
   }
 
+  /**
+   * Identifies if the sender frame is the same as the focused field's frame.
+   *
+   * @param sender - The sender of the message
+   */
+  private senderFrameHasFocusedField(sender: chrome.runtime.MessageSender) {
+    return sender.frameId === this.focusedFieldData?.frameId;
+  }
+
   /**
    * Triggers when a scroll or resize event occurs within a tab. Will reposition the inline menu
    * if the focused field is within the viewport.
diff --git a/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts b/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts
index 6145dbfdc0..15eeff75cd 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.spec.ts
@@ -1986,6 +1986,19 @@ describe("AutofillOverlayContentService", () => {
         expect(autofillFieldFocusSpy).not.toHaveBeenCalled();
         expect(nextFocusableElement.focus).toHaveBeenCalled();
       });
+
+      it("focuses the most recently focused input field if no other tabbable elements are found", async () => {
+        autofillOverlayContentService["focusableElements"] = [];
+        findTabsSpy.mockReturnValue([]);
+
+        sendMockExtensionMessage({
+          command: "redirectAutofillInlineMenuFocusOut",
+          data: { direction: RedirectFocusDirection.Next },
+        });
+        await flushPromises();
+
+        expect(autofillFieldFocusSpy).toHaveBeenCalled();
+      });
     });
 
     describe("updateAutofillInlineMenuVisibility message handler", () => {
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 0881ecba1e..9a45403edc 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -338,7 +338,12 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
 
     const indexOffset = direction === RedirectFocusDirection.Previous ? -1 : 1;
     const redirectFocusElement = this.focusableElements[focusedElementIndex + indexOffset];
-    redirectFocusElement?.focus();
+    if (redirectFocusElement) {
+      redirectFocusElement.focus();
+      return;
+    }
+
+    this.focusMostRecentlyFocusedField();
   }
 
   /**
@@ -1418,8 +1423,8 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       focusedFieldRectsTop + this.focusedFieldData?.focusedFieldRects?.height;
     const viewportHeight = globalThis.innerHeight + globalThis.scrollY;
     return (
-      focusedFieldRectsTop &&
-      focusedFieldRectsTop > 0 &&
+      !globalThis.isNaN(focusedFieldRectsTop) &&
+      focusedFieldRectsTop >= 0 &&
       focusedFieldRectsTop < viewportHeight &&
       focusedFieldRectsBottom < viewportHeight
     );