diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 5e79585306..8b8ec47e89 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -94,15 +94,10 @@ export type BackgroundOnMessageHandlerParams = BackgroundMessageParam & Backgrou
 
 export type OverlayBackgroundExtensionMessageHandlers = {
   [key: string]: CallableFunction;
-  triggerAutofillOverlayReposition: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   checkIsInlineMenuCiphersPopulated: ({ sender }: BackgroundSenderParam) => void;
-  updateFocusedFieldData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
-  updateIsFieldCurrentlyFocused: ({ message }: BackgroundMessageParam) => void;
-  checkIsFieldCurrentlyFocused: () => boolean;
   updateIsFieldCurrentlyFilling: ({ message }: BackgroundMessageParam) => void;
   checkIsFieldCurrentlyFilling: () => boolean;
   getAutofillInlineMenuVisibility: () => void;
-  openAutofillInlineMenu: () => void;
   closeAutofillInlineMenu: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   checkAutofillInlineMenuFocused: () => void;
   focusAutofillInlineMenuList: () => void;
@@ -132,7 +127,6 @@ export type OverlayPortMessage = OverlayBackgroundExtensionMessage & {
   direction?: string;
   inlineMenuCipherId?: string;
 };
-
 export type PortMessageParam = {
   message: OverlayPortMessage;
 };
@@ -145,6 +139,10 @@ export type OverlayContentScriptPortMessageHandlers = {
   [key: string]: CallableFunction;
   autofillOverlayElementClosed: ({ message, port }: PortOnMessageHandlerParams) => void;
   autofillOverlayAddNewVaultItem: ({ message, port }: PortOnMessageHandlerParams) => void;
+  triggerAutofillOverlayReposition: ({ port }: PortConnectionParam) => void;
+  updateFocusedFieldData: ({ message, port }: PortOnMessageHandlerParams) => void;
+  updateIsFieldCurrentlyFocused: ({ message }: PortMessageParam) => void;
+  openAutofillInlineMenu: () => void;
 };
 
 export type InlineMenuButtonPortMessageHandlers = {
diff --git a/apps/browser/src/autofill/background/overlay.background.spec.ts b/apps/browser/src/autofill/background/overlay.background.spec.ts
index f71b387102..9ad8fdd598 100644
--- a/apps/browser/src/autofill/background/overlay.background.spec.ts
+++ b/apps/browser/src/autofill/background/overlay.background.spec.ts
@@ -790,24 +790,6 @@ describe("OverlayBackground", () => {
       });
     });
 
-    describe("checkIsFieldCurrentlyFocused message handler", () => {
-      it("returns true when a form field is currently focused", async () => {
-        sendMockExtensionMessage({
-          command: "updateIsFieldCurrentlyFocused",
-          isFieldCurrentlyFocused: true,
-        });
-
-        sendMockExtensionMessage(
-          { command: "checkIsFieldCurrentlyFocused" },
-          mock<chrome.runtime.MessageSender>(),
-          sendResponse,
-        );
-        await flushPromises();
-
-        expect(sendResponse).toHaveBeenCalledWith(true);
-      });
-    });
-
     describe("checkIsFieldCurrentlyFilling message handler", () => {
       it("returns true if autofill is currently running", async () => {
         sendMockExtensionMessage({
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index bbf5d2ccee..38343ff0b4 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -76,16 +76,11 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   private isFieldCurrentlyFilling: boolean = false;
   private iconsServerUrl: string;
   private readonly extensionMessageHandlers: OverlayBackgroundExtensionMessageHandlers = {
-    triggerAutofillOverlayReposition: ({ sender }) => this.triggerOverlayReposition(sender),
     checkIsInlineMenuCiphersPopulated: ({ sender }) =>
       this.checkIsInlineMenuCiphersPopulated(sender),
-    updateFocusedFieldData: ({ message, sender }) => this.setFocusedFieldData(message, sender),
-    updateIsFieldCurrentlyFocused: ({ message }) => this.updateIsFieldCurrentlyFocused(message),
-    checkIsFieldCurrentlyFocused: () => this.checkIsFieldCurrentlyFocused(),
     updateIsFieldCurrentlyFilling: ({ message }) => this.updateIsFieldCurrentlyFilling(message),
     checkIsFieldCurrentlyFilling: () => this.checkIsFieldCurrentlyFilling(),
     getAutofillInlineMenuVisibility: () => this.getInlineMenuVisibility(),
-    openAutofillInlineMenu: () => this.openInlineMenu(false),
     closeAutofillInlineMenu: ({ message, sender }) => this.closeInlineMenu(sender, message),
     checkAutofillInlineMenuFocused: () => this.checkInlineMenuFocused(),
     focusAutofillInlineMenuList: () => this.focusInlineMenuList(),
@@ -111,6 +106,10 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   private readonly contentScriptPortMessageHandlers: OverlayContentScriptPortMessageHandlers = {
     autofillOverlayElementClosed: ({ message, port }) => this.overlayElementClosed(message, port),
     autofillOverlayAddNewVaultItem: ({ message, port }) => this.addNewVaultItem(message, port),
+    triggerAutofillOverlayReposition: ({ port }) => this.triggerOverlayReposition(port),
+    updateFocusedFieldData: ({ message, port }) => this.setFocusedFieldData(message, port),
+    updateIsFieldCurrentlyFocused: ({ message }) => this.updateIsFieldCurrentlyFocused(message),
+    openAutofillInlineMenu: () => this.openInlineMenu(false),
   };
   private readonly inlineMenuButtonPortMessageHandlers: InlineMenuButtonPortMessageHandlers = {
     triggerDelayedAutofillInlineMenuClosure: ({ port }) => this.triggerDelayedInlineMenuClosure(),
@@ -614,13 +613,13 @@ export class OverlayBackground implements OverlayBackgroundInterface {
    * the list and button ports and sets them to null.
    *
    * @param overlayElement - The overlay element that was closed, either the list or button
-   * @param port - The port that sent the message
+   * @param sender - The sender of the port message
    */
   private overlayElementClosed(
     { overlayElement }: OverlayBackgroundExtensionMessage,
-    port: chrome.runtime.Port,
+    { sender }: chrome.runtime.Port,
   ) {
-    if (port.sender.tab.id !== this.focusedFieldData?.tabId) {
+    if (sender.tab.id !== this.focusedFieldData?.tabId) {
       this.expiredPorts.forEach((port) => port.disconnect());
       this.expiredPorts = [];
       return;
@@ -762,11 +761,11 @@ export class OverlayBackground implements OverlayBackgroundInterface {
    * Sets the focused field data to the data passed in the extension message.
    *
    * @param focusedFieldData - Contains the rects and styles of the focused field.
-   * @param sender - The sender of the extension message
+   * @param sender - The sender of the port message
    */
   private setFocusedFieldData(
     { focusedFieldData }: OverlayBackgroundExtensionMessage,
-    sender: chrome.runtime.MessageSender,
+    { sender }: chrome.runtime.Port,
   ) {
     if (this.focusedFieldData?.frameId && this.focusedFieldData.frameId !== sender.frameId) {
       void BrowserApi.tabSendMessage(
@@ -1015,9 +1014,12 @@ export class OverlayBackground implements OverlayBackgroundInterface {
    * data captured in the extension message.
    *
    * @param login - The login data captured from the extension message
-   * @param port - The content script port
+   * @param sender - The sender of the port message
    */
-  private async addNewVaultItem({ login }: OverlayAddNewItemMessage, port: chrome.runtime.Port) {
+  private async addNewVaultItem(
+    { login }: OverlayAddNewItemMessage,
+    { sender }: chrome.runtime.Port,
+  ) {
     if (!login) {
       return;
     }
@@ -1041,7 +1043,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       collectionIds: cipherView.collectionIds,
     });
 
-    await this.openAddEditVaultItemPopout(port.sender.tab, { cipherId: cipherView.id });
+    await this.openAddEditVaultItemPopout(sender.tab, { cipherId: cipherView.id });
     await BrowserApi.sendMessage("inlineAutofillMenuRefreshAddEditCipher");
   }
 
@@ -1054,13 +1056,6 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     this.isFieldCurrentlyFocused = message.isFieldCurrentlyFocused;
   }
 
-  /**
-   * Allows a content script to check if a form field setup for the inline menu is currently focused.
-   */
-  private checkIsFieldCurrentlyFocused() {
-    return this.isFieldCurrentlyFocused;
-  }
-
   /**
    * Updates the property that identifies if a form field is currently being autofilled.
    *
@@ -1361,7 +1356,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     }
   };
 
-  private async triggerOverlayReposition(sender: chrome.runtime.MessageSender) {
+  private async triggerOverlayReposition({ sender }: chrome.runtime.Port) {
     if (await this.checkShouldRepositionInlineMenu(sender)) {
       await this.toggleInlineMenuHidden({ isInlineMenuHidden: true }, sender);
       this.calculateInlineMenuPositionSubject.next(sender);
diff --git a/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts b/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts
index e44cc2e3bf..13e7407c01 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts
@@ -425,7 +425,7 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
    */
   private sendPortMessage(
     command: string,
-    message: Omit<AutofillOverlayContentExtensionMessage, "command">,
+    message: Omit<AutofillOverlayContentExtensionMessage, "command"> = {},
   ) {
     this.port.postMessage({ command, ...message });
   }
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 a168ebe72c..cceeddbac8 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
@@ -1,6 +1,7 @@
 import { AuthenticationStatus } from "@bitwarden/common/auth/enums/authentication-status";
 
 import {
+  FocusedFieldData,
   OverlayAddNewItemMessage,
   SubFrameOffsetData,
 } from "../../background/abstractions/overlay.background";
@@ -41,6 +42,8 @@ export type AutofillOverlayContentExtensionMessageHandlers = {
 export type AutofillOverlayContentExtensionMessage = {
   command: string;
   overlayElement?: AutofillOverlayElementType;
+  focusedFieldData?: FocusedFieldData;
+  isFieldCurrentlyFocused?: boolean;
 } & OverlayAddNewItemMessage;
 
 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 4030ec6fe5..2fbf281275 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -347,7 +347,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
    * is currently focused.
    */
   private handleFormFieldBlurEvent = () => {
-    void this.sendExtensionMessage("updateIsFieldCurrentlyFocused", {
+    this.sendPortMessage("updateIsFieldCurrentlyFocused", {
       isFieldCurrentlyFocused: false,
     });
     void this.sendExtensionMessage("checkAutofillInlineMenuFocused");
@@ -371,7 +371,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     }
 
     if (eventCode === "Enter" && !(await this.isFieldCurrentlyFilling())) {
-      void this.handleOverlayRepositionEvent();
+      this.handleOverlayRepositionEvent();
       return;
     }
 
@@ -511,7 +511,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       return;
     }
 
-    await this.sendExtensionMessage("updateIsFieldCurrentlyFocused", {
+    this.sendPortMessage("updateIsFieldCurrentlyFocused", {
       isFieldCurrentlyFocused: true,
     });
     if (this.userInteractionEventTimeout) {
@@ -540,7 +540,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       return;
     }
 
-    void this.sendExtensionMessage("openAutofillInlineMenu");
+    this.sendPortMessage("openAutofillInlineMenu");
   }
 
   /**
@@ -621,7 +621,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
       focusedFieldRects: { width, height, top, left },
     };
 
-    await this.sendExtensionMessage("updateFocusedFieldData", {
+    this.sendPortMessage("updateFocusedFieldData", {
       focusedFieldData: this.focusedFieldData,
     });
   }
@@ -1071,8 +1071,8 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
    * Handles the resize or scroll events that enact
    * repositioning of existing overlay elements.
    */
-  private handleOverlayRepositionEvent = async () => {
-    await this.sendExtensionMessage("triggerAutofillOverlayReposition");
+  private handleOverlayRepositionEvent = () => {
+    this.sendPortMessage("triggerAutofillOverlayReposition");
   };
 
   private setupRebuildSubFrameOffsetsListeners = () => {
@@ -1130,7 +1130,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
    */
   private sendPortMessage(
     command: string,
-    message: Omit<AutofillOverlayContentExtensionMessage, "command">,
+    message: Omit<AutofillOverlayContentExtensionMessage, "command"> = {},
   ) {
     this.port.postMessage({ command, ...message });
   }