diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 8b8ec47e89..3313d3405c 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -98,9 +98,7 @@ export type OverlayBackgroundExtensionMessageHandlers = {
   updateIsFieldCurrentlyFilling: ({ message }: BackgroundMessageParam) => void;
   checkIsFieldCurrentlyFilling: () => boolean;
   getAutofillInlineMenuVisibility: () => void;
-  closeAutofillInlineMenu: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
-  checkAutofillInlineMenuFocused: () => void;
-  focusAutofillInlineMenuList: () => void;
+
   updateAutofillInlineMenuPosition: ({
     message,
     sender,
@@ -143,10 +141,14 @@ export type OverlayContentScriptPortMessageHandlers = {
   updateFocusedFieldData: ({ message, port }: PortOnMessageHandlerParams) => void;
   updateIsFieldCurrentlyFocused: ({ message }: PortMessageParam) => void;
   openAutofillInlineMenu: () => void;
+  closeAutofillInlineMenu: ({ message, port }: PortOnMessageHandlerParams) => void;
+  checkAutofillInlineMenuFocused: () => void;
+  focusAutofillInlineMenuList: () => void;
 };
 
 export type InlineMenuButtonPortMessageHandlers = {
   [key: string]: CallableFunction;
+  closeAutofillInlineMenu: ({ message, port }: PortOnMessageHandlerParams) => void;
   triggerDelayedAutofillInlineMenuClosure: ({ port }: PortConnectionParam) => void;
   autofillInlineMenuButtonClicked: ({ port }: PortConnectionParam) => void;
   autofillInlineMenuBlurred: () => void;
@@ -156,6 +158,7 @@ export type InlineMenuButtonPortMessageHandlers = {
 
 export type InlineMenuListPortMessageHandlers = {
   [key: string]: CallableFunction;
+  closeAutofillInlineMenu: ({ message, port }: PortOnMessageHandlerParams) => void;
   checkAutofillInlineMenuButtonFocused: () => void;
   autofillInlineMenuBlurred: () => void;
   unlockVault: ({ port }: PortConnectionParam) => void;
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 38343ff0b4..9d948dd26f 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -81,9 +81,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     updateIsFieldCurrentlyFilling: ({ message }) => this.updateIsFieldCurrentlyFilling(message),
     checkIsFieldCurrentlyFilling: () => this.checkIsFieldCurrentlyFilling(),
     getAutofillInlineMenuVisibility: () => this.getInlineMenuVisibility(),
-    closeAutofillInlineMenu: ({ message, sender }) => this.closeInlineMenu(sender, message),
-    checkAutofillInlineMenuFocused: () => this.checkInlineMenuFocused(),
-    focusAutofillInlineMenuList: () => this.focusInlineMenuList(),
+
     updateAutofillInlineMenuPosition: ({ message, sender }) =>
       this.updateInlineMenuPosition(message, sender),
     toggleAutofillInlineMenuHidden: ({ message, sender }) =>
@@ -110,8 +108,12 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     updateFocusedFieldData: ({ message, port }) => this.setFocusedFieldData(message, port),
     updateIsFieldCurrentlyFocused: ({ message }) => this.updateIsFieldCurrentlyFocused(message),
     openAutofillInlineMenu: () => this.openInlineMenu(false),
+    closeAutofillInlineMenu: ({ message, port }) => this.closeInlineMenu(port.sender, message),
+    checkAutofillInlineMenuFocused: () => this.checkInlineMenuFocused(),
+    focusAutofillInlineMenuList: () => this.focusInlineMenuList(),
   };
   private readonly inlineMenuButtonPortMessageHandlers: InlineMenuButtonPortMessageHandlers = {
+    closeAutofillInlineMenu: ({ message, port }) => this.closeInlineMenu(port.sender, message),
     triggerDelayedAutofillInlineMenuClosure: ({ port }) => this.triggerDelayedInlineMenuClosure(),
     autofillInlineMenuButtonClicked: ({ port }) => this.handleInlineMenuButtonClicked(port),
     autofillInlineMenuBlurred: () => this.checkInlineMenuListFocused(),
@@ -120,6 +122,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     updateAutofillInlineMenuColorScheme: () => this.updateInlineMenuButtonColorScheme(),
   };
   private readonly inlineMenuListPortMessageHandlers: InlineMenuListPortMessageHandlers = {
+    closeAutofillInlineMenu: ({ message, port }) => this.closeInlineMenu(port.sender, message),
     checkAutofillInlineMenuButtonFocused: () => this.checkInlineMenuButtonFocused(),
     autofillInlineMenuBlurred: () => this.checkInlineMenuButtonFocused(),
     unlockVault: ({ port }) => this.unlockVault(port),
diff --git a/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.ts b/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.ts
index a8d4c7354d..997836dd36 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.ts
@@ -1,7 +1,7 @@
 import { EVENTS } from "@bitwarden/common/autofill/constants";
 import { ThemeType } from "@bitwarden/common/platform/enums";
 
-import { sendExtensionMessage, setElementStyles } from "../../../utils";
+import { setElementStyles } from "../../../utils";
 import {
   BackgroundPortMessageHandlers,
   AutofillInlineMenuIframeService as AutofillInlineMenuIframeServiceInterface,
@@ -10,7 +10,6 @@ import {
 
 export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframeServiceInterface {
   private readonly setElementStyles = setElementStyles;
-  private readonly sendExtensionMessage = sendExtensionMessage;
   private port: chrome.runtime.Port | null = null;
   private portKey: string;
   private iframeMutationObserver: MutationObserver;
@@ -305,7 +304,7 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
    * mutation observer is triggered excessively.
    */
   private forceCloseInlineMenu() {
-    void this.sendExtensionMessage("closeAutofillInlineMenu", { forceClose: true });
+    void this.port.postMessage({ command: "closeAutofillInlineMenu", forceClose: true });
   }
 
   private handleFadeInInlineMenuIframe() {
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 cceeddbac8..853778ed97 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
@@ -44,6 +44,7 @@ export type AutofillOverlayContentExtensionMessage = {
   overlayElement?: AutofillOverlayElementType;
   focusedFieldData?: FocusedFieldData;
   isFieldCurrentlyFocused?: boolean;
+  forceCloseInlineMenu?: boolean;
 } & OverlayAddNewItemMessage;
 
 export interface AutofillOverlayContentService {
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 da9e7f6200..0b77f7e051 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
@@ -905,17 +905,6 @@ describe("AutofillOverlayContentService", () => {
       });
     });
 
-    it("clears the user interaction timeout", async () => {
-      jest.useFakeTimers();
-      const clearTimeoutSpy = jest.spyOn(globalThis, "clearTimeout");
-      autofillOverlayContentService["userInteractionEventTimeout"] = setTimeout(jest.fn(), 123);
-
-      globalThis.dispatchEvent(new Event(EVENTS.SCROLL));
-      await flushPromises();
-
-      expect(clearTimeoutSpy).toHaveBeenCalledWith(expect.anything());
-    });
-
     it("removes the overlay completely if the field is not focused", async () => {
       jest.useFakeTimers();
       jest
@@ -1695,14 +1684,6 @@ describe("AutofillOverlayContentService", () => {
       autofillOverlayContentService["mostRecentlyFocusedField"] = autofillFieldElement;
     });
 
-    it("clears the user interaction event timeout", () => {
-      jest.spyOn(autofillOverlayContentService as any, "clearUserInteractionEventTimeout");
-
-      autofillOverlayContentService.destroy();
-
-      expect(autofillOverlayContentService["clearUserInteractionEventTimeout"]).toHaveBeenCalled();
-    });
-
     it("de-registers all global event listeners", () => {
       jest.spyOn(globalThis.document, "removeEventListener");
       jest.spyOn(globalThis, "removeEventListener");
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 2fbf281275..07d03b2341 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -54,11 +54,8 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
   private focusableElements: FocusableElement[] = [];
   private mostRecentlyFocusedField: ElementWithOpId<FormFieldElement>;
   private focusedFieldData: FocusedFieldData;
-  private userInteractionEventTimeout: number | NodeJS.Timeout;
-  private recalculateSubFrameOffsetsTimeout: number | NodeJS.Timeout;
   private closeInlineMenuOnRedirectTimeout: number | NodeJS.Timeout;
   private focusInlineMenuListTimeout: number | NodeJS.Timeout;
-  private closeInlineMenuOnFilledFieldTimeout: number | NodeJS.Timeout;
   private eventHandlersMemo: { [key: string]: EventListener } = {};
   private readonly extensionMessageHandlers: AutofillOverlayContentExtensionMessageHandlers = {
     openAutofillInlineMenu: ({ message }) => this.openInlineMenu(message),
@@ -207,7 +204,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     this.mostRecentlyFocusedField?.blur();
 
     if (isClosingInlineMenu) {
-      void this.sendExtensionMessage("closeAutofillInlineMenu");
+      this.sendPortMessage("closeAutofillInlineMenu");
     }
   }
 
@@ -252,7 +249,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     if (direction === RedirectFocusDirection.Current) {
       this.focusMostRecentlyFocusedField();
       this.closeInlineMenuOnRedirectTimeout = globalThis.setTimeout(
-        () => void this.sendExtensionMessage("closeAutofillInlineMenu"),
+        () => this.sendPortMessage("closeAutofillInlineMenu"),
         100,
       );
       return;
@@ -350,7 +347,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     this.sendPortMessage("updateIsFieldCurrentlyFocused", {
       isFieldCurrentlyFocused: false,
     });
-    void this.sendExtensionMessage("checkAutofillInlineMenuFocused");
+    this.sendPortMessage("checkAutofillInlineMenuFocused");
   };
 
   /**
@@ -364,7 +361,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
   private handleFormFieldKeyupEvent = async (event: KeyboardEvent) => {
     const eventCode = event.code;
     if (eventCode === "Escape") {
-      void this.sendExtensionMessage("closeAutofillInlineMenu", {
+      this.sendPortMessage("closeAutofillInlineMenu", {
         forceCloseInlineMenu: true,
       });
       return;
@@ -394,13 +391,13 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       await this.updateMostRecentlyFocusedField(this.mostRecentlyFocusedField);
       this.openInlineMenu({ isOpeningFullInlineMenu: true });
       this.focusInlineMenuListTimeout = globalThis.setTimeout(
-        () => this.sendExtensionMessage("focusAutofillInlineMenuList"),
+        () => this.sendPortMessage("focusAutofillInlineMenuList"),
         125,
       );
       return;
     }
 
-    void this.sendExtensionMessage("focusAutofillInlineMenuList");
+    this.sendPortMessage("focusAutofillInlineMenuList");
   }
 
   /**
@@ -430,7 +427,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     this.storeModifiedFormElement(formFieldElement);
 
     if (await this.hideInlineMenuListOnFilledField(formFieldElement)) {
-      void this.sendExtensionMessage("closeAutofillInlineMenu", {
+      this.sendPortMessage("closeAutofillInlineMenu", {
         overlayElement: AutofillOverlayElement.List,
         forceCloseInlineMenu: true,
       });
@@ -514,13 +511,6 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     this.sendPortMessage("updateIsFieldCurrentlyFocused", {
       isFieldCurrentlyFocused: true,
     });
-    if (this.userInteractionEventTimeout) {
-      this.clearUserInteractionEventTimeout();
-      void this.toggleInlineMenuHidden(false, true);
-      void this.sendExtensionMessage("closeAutofillInlineMenu", {
-        forceCloseInlineMenu: true,
-      });
-    }
     const initiallyFocusedField = this.mostRecentlyFocusedField;
     await this.updateMostRecentlyFocusedField(formFieldElement);
 
@@ -529,7 +519,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       (initiallyFocusedField !== this.mostRecentlyFocusedField &&
         (await this.hideInlineMenuListOnFilledField(formFieldElement as FillableFormFieldElement)))
     ) {
-      await this.sendExtensionMessage("closeAutofillInlineMenu", {
+      this.sendPortMessage("closeAutofillInlineMenu", {
         overlayElement: AutofillOverlayElement.List,
         forceCloseInlineMenu: true,
       });
@@ -1017,7 +1007,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     }
 
     this.unsetMostRecentlyFocusedField();
-    void this.sendExtensionMessage("closeAutofillInlineMenu", {
+    this.sendPortMessage("closeAutofillInlineMenu", {
       forceCloseInlineMenu: true,
     });
   };
@@ -1135,32 +1125,6 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     this.port.postMessage({ command, ...message });
   }
 
-  /**
-   * Clears the user interaction event timeout. This is used to ensure that
-   * the overlay is not repositioned while the user is interacting with it.
-   */
-  private clearUserInteractionEventTimeout() {
-    if (this.userInteractionEventTimeout) {
-      globalThis.clearTimeout(this.userInteractionEventTimeout);
-      this.userInteractionEventTimeout = null;
-    }
-  }
-
-  private clearCloseInlineMenuOnFilledFieldTimeout() {
-    if (this.closeInlineMenuOnFilledFieldTimeout) {
-      globalThis.clearTimeout(this.closeInlineMenuOnFilledFieldTimeout);
-    }
-  }
-
-  /**
-   * Clears the timeout that facilitates recalculating the sub frame offsets.
-   */
-  private clearRecalculateSubFrameOffsetsTimeout() {
-    if (this.recalculateSubFrameOffsetsTimeout) {
-      globalThis.clearTimeout(this.recalculateSubFrameOffsetsTimeout);
-    }
-  }
-
   private clearFocusInlineMenuListTimeout() {
     if (this.focusInlineMenuListTimeout) {
       globalThis.clearTimeout(this.focusInlineMenuListTimeout);
@@ -1174,9 +1138,6 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
   }
 
   private clearAllTimeouts() {
-    this.clearUserInteractionEventTimeout();
-    this.clearCloseInlineMenuOnFilledFieldTimeout();
-    this.clearRecalculateSubFrameOffsetsTimeout();
     this.clearFocusInlineMenuListTimeout();
     this.clearCloseInlineMenuOnRedirectTimeout();
   }