diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index f08176469c..65289c02da 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -94,7 +94,7 @@ export type OverlayBackgroundExtensionMessageHandlers = {
   [key: string]: CallableFunction;
   autofillOverlayElementClosed: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   autofillOverlayAddNewVaultItem: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
-  checkIsOverlayLoginCiphersPopulated: ({ sender }: BackgroundSenderParam) => void;
+  checkIsInlineMenuCiphersPopulated: ({ sender }: BackgroundSenderParam) => void;
   updateFocusedFieldData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
   updateIsFieldCurrentlyFocused: ({ message }: BackgroundMessageParam) => void;
   checkIsFieldCurrentlyFocused: () => boolean;
diff --git a/apps/browser/src/autofill/background/overlay.background.spec.ts b/apps/browser/src/autofill/background/overlay.background.spec.ts
index b6f05415c0..e1da0a1c4a 100644
--- a/apps/browser/src/autofill/background/overlay.background.spec.ts
+++ b/apps/browser/src/autofill/background/overlay.background.spec.ts
@@ -32,9 +32,14 @@ import { CipherView } from "@bitwarden/common/vault/models/view/cipher.view";
 
 import { BrowserApi } from "../../platform/browser/browser-api";
 import { BrowserPlatformUtilsService } from "../../platform/services/platform-utils/browser-platform-utils.service";
-import { AutofillOverlayElement } from "../enums/autofill-overlay.enum";
+import { AutofillOverlayElement, AutofillOverlayPort } from "../enums/autofill-overlay.enum";
 import { AutofillService } from "../services/abstractions/autofill.service";
-import { createChromeTabMock, createAutofillPageDetailsMock } from "../spec/autofill-mocks";
+import {
+  createChromeTabMock,
+  createAutofillPageDetailsMock,
+  createPortSpyMock,
+  createFocusedFieldDataMock,
+} from "../spec/autofill-mocks";
 import { flushPromises, sendMockExtensionMessage } from "../spec/testing-utils";
 
 import {
@@ -47,6 +52,7 @@ import { OverlayBackground } from "./overlay.background";
 
 describe("OverlayBackground", () => {
   const mockUserId = Utils.newGuid() as UserId;
+  const sendResponse = jest.fn();
   let accountService: FakeAccountService;
   let fakeStateProvider: FakeStateProvider;
   let showFaviconsMock$: BehaviorSubject<boolean>;
@@ -70,8 +76,26 @@ describe("OverlayBackground", () => {
   let subFrameOffsetsSpy: SubFrameOffsetsForTab;
   let getFrameDetailsSpy: jest.SpyInstance;
   let tabsSendMessageSpy: jest.SpyInstance;
+  let sendMessageSpy: jest.SpyInstance;
   let getTabFromCurrentWindowIdSpy: jest.SpyInstance;
+  let buttonPortSpy: chrome.runtime.Port;
+  let listPortSpy: chrome.runtime.Port;
+
   let getFrameCounter: number = 2;
+  async function initOverlayElementPorts(options = { initList: true, initButton: true }) {
+    const { initList, initButton } = options;
+    if (initButton) {
+      await overlayBackground["handlePortOnConnect"](createPortSpyMock(AutofillOverlayPort.Button));
+      buttonPortSpy = overlayBackground["inlineMenuButtonPort"];
+    }
+
+    if (initList) {
+      await overlayBackground["handlePortOnConnect"](createPortSpyMock(AutofillOverlayPort.List));
+      listPortSpy = overlayBackground["inlineMenuListPort"];
+    }
+
+    return { buttonPortSpy, listPortSpy };
+  }
 
   beforeEach(() => {
     accountService = mockAccountServiceWith(mockUserId);
@@ -125,6 +149,7 @@ describe("OverlayBackground", () => {
       });
     });
     tabsSendMessageSpy = jest.spyOn(BrowserApi, "tabSendMessage");
+    sendMessageSpy = jest.spyOn(BrowserApi, "sendMessage");
     getTabFromCurrentWindowIdSpy = jest.spyOn(BrowserApi, "getTabFromCurrentWindowId");
 
     void overlayBackground.init();
@@ -349,11 +374,17 @@ describe("OverlayBackground", () => {
       beforeEach(() => {
         sender = mock<chrome.runtime.MessageSender>({ tab, frameId: middleFrameId });
         jest.useFakeTimers();
-        overlayBackground["isFieldCurrentlyFocused"] = true;
+        sendMockExtensionMessage({
+          command: "updateIsFieldCurrentlyFocused",
+          isFieldCurrentlyFocused: true,
+        });
       });
 
       it("skips updating the position of either inline menu element if a field is not currently focused", async () => {
-        overlayBackground["isFieldCurrentlyFocused"] = false;
+        sendMockExtensionMessage({
+          command: "updateIsFieldCurrentlyFocused",
+          isFieldCurrentlyFocused: false,
+        });
 
         sendMockExtensionMessage({ command: "rebuildSubFrameOffsets" }, sender);
         await flushInlineMenuUpdatePromises();
@@ -430,7 +461,7 @@ describe("OverlayBackground", () => {
     });
   });
 
-  describe("updateOverlayCiphers", () => {
+  describe("updating the overlay ciphers", () => {
     const url = "https://jest-testing-website.com";
     const tab = createChromeTabMock({ url });
     const cipher1 = mock<CipherView>({
@@ -480,7 +511,7 @@ describe("OverlayBackground", () => {
       expect(BrowserApi.getTabFromCurrentWindowId).toHaveBeenCalled();
       expect(cipherService.getAllDecryptedForUrl).toHaveBeenCalledWith(url);
       expect(cipherService.sortCiphersByLastUsedThenName).toHaveBeenCalled();
-      expect(overlayBackground["overlayLoginCiphers"]).toStrictEqual(
+      expect(overlayBackground["inlineMenuCiphers"]).toStrictEqual(
         new Map([
           ["overlay-cipher-0", cipher2],
           ["overlay-cipher-1", cipher1],
@@ -535,4 +566,230 @@ describe("OverlayBackground", () => {
       });
     });
   });
+
+  describe("extension message handlers", () => {
+    describe("autofillOverlayElementClosed message handler", () => {
+      beforeEach(async () => {
+        await initOverlayElementPorts();
+      });
+
+      it("disconnects any expired ports if the sender is not from the same page as the most recently focused field", () => {
+        const port1 = mock<chrome.runtime.Port>();
+        const port2 = mock<chrome.runtime.Port>();
+        overlayBackground["expiredPorts"] = [port1, port2];
+        const sender = mock<chrome.runtime.MessageSender>({ tab: { id: 1 } });
+        const focusedFieldData = createFocusedFieldDataMock({ tabId: 2 });
+        sendMockExtensionMessage({ command: "updateFocusedFieldData", focusedFieldData });
+
+        sendMockExtensionMessage(
+          {
+            command: "autofillOverlayElementClosed",
+            overlayElement: AutofillOverlayElement.Button,
+          },
+          sender,
+        );
+
+        expect(port1.disconnect).toHaveBeenCalled();
+        expect(port2.disconnect).toHaveBeenCalled();
+      });
+
+      it("disconnects the button element port", () => {
+        sendMockExtensionMessage({
+          command: "autofillOverlayElementClosed",
+          overlayElement: AutofillOverlayElement.Button,
+        });
+
+        expect(buttonPortSpy.disconnect).toHaveBeenCalled();
+      });
+
+      it("disconnects the list element port", () => {
+        sendMockExtensionMessage({
+          command: "autofillOverlayElementClosed",
+          overlayElement: AutofillOverlayElement.List,
+        });
+
+        expect(listPortSpy.disconnect).toHaveBeenCalled();
+      });
+    });
+
+    describe("autofillOverlayAddNewVaultItem message handler", () => {
+      let sender: chrome.runtime.MessageSender;
+      let openAddEditVaultItemPopoutSpy: jest.SpyInstance;
+
+      beforeEach(() => {
+        sender = mock<chrome.runtime.MessageSender>({ tab: { id: 1 } });
+        openAddEditVaultItemPopoutSpy = jest
+          .spyOn(overlayBackground as any, "openAddEditVaultItemPopout")
+          .mockImplementation();
+      });
+
+      it("will not open the add edit popout window if the message does not have a login cipher provided", () => {
+        sendMockExtensionMessage({ command: "autofillOverlayAddNewVaultItem" }, sender);
+
+        expect(cipherService.setAddEditCipherInfo).not.toHaveBeenCalled();
+        expect(openAddEditVaultItemPopoutSpy).not.toHaveBeenCalled();
+      });
+
+      it("will open the add edit popout window after creating a new cipher", async () => {
+        sendMockExtensionMessage(
+          {
+            command: "autofillOverlayAddNewVaultItem",
+            login: {
+              uri: "https://tacos.com",
+              hostname: "",
+              username: "username",
+              password: "password",
+            },
+          },
+          sender,
+        );
+        await flushPromises();
+
+        expect(cipherService.setAddEditCipherInfo).toHaveBeenCalled();
+        expect(sendMessageSpy).toHaveBeenCalledWith("inlineAutofillMenuRefreshAddEditCipher");
+        expect(openAddEditVaultItemPopoutSpy).toHaveBeenCalled();
+      });
+    });
+
+    describe("checkIsInlineMenuCiphersPopulated message handler", () => {
+      let focusedFieldData: FocusedFieldData;
+
+      beforeEach(() => {
+        focusedFieldData = createFocusedFieldDataMock();
+        sendMockExtensionMessage(
+          { command: "updateFocusedFieldData", focusedFieldData },
+          mock<chrome.runtime.MessageSender>({ tab: { id: 2 }, frameId: 0 }),
+        );
+      });
+
+      it("returns false if the sender's tab id is not equal to the focused field's tab id", async () => {
+        const sender = mock<chrome.runtime.MessageSender>({ tab: { id: 1 } });
+
+        sendMockExtensionMessage(
+          { command: "checkIsInlineMenuCiphersPopulated" },
+          sender,
+          sendResponse,
+        );
+        await flushPromises();
+
+        expect(sendResponse).toHaveBeenCalledWith(false);
+      });
+
+      it("returns false if the overlay login cipher are not populated", () => {});
+
+      it("returns true if the overlay login ciphers are populated", async () => {
+        overlayBackground["inlineMenuCiphers"] = new Map([
+          ["overlay-cipher-0", mock<CipherView>()],
+        ]);
+
+        sendMockExtensionMessage(
+          { command: "checkIsInlineMenuCiphersPopulated" },
+          mock<chrome.runtime.MessageSender>({ tab: { id: 2 } }),
+          sendResponse,
+        );
+        await flushPromises();
+
+        expect(sendResponse).toHaveBeenCalledWith(true);
+      });
+    });
+
+    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({
+          command: "updateIsFieldCurrentlyFilling",
+          isFieldCurrentlyFilling: true,
+        });
+
+        sendMockExtensionMessage(
+          { command: "checkIsFieldCurrentlyFilling" },
+          mock<chrome.runtime.MessageSender>(),
+          sendResponse,
+        );
+        await flushPromises();
+
+        expect(sendResponse).toHaveBeenCalledWith(true);
+      });
+    });
+
+    describe("getAutofillInlineMenuVisibility message handler", () => {
+      it("returns the current inline menu visibility setting", async () => {
+        sendMockExtensionMessage(
+          { command: "getAutofillInlineMenuVisibility" },
+          mock<chrome.runtime.MessageSender>(),
+          sendResponse,
+        );
+        await flushPromises();
+
+        expect(sendResponse).toHaveBeenCalledWith(AutofillOverlayVisibility.OnFieldFocus);
+      });
+    });
+
+    describe("openAutofillInlineMenu", () => {
+      let sender: chrome.runtime.MessageSender;
+
+      beforeEach(() => {
+        sender = mock<chrome.runtime.MessageSender>({ tab: { id: 1 } });
+        getTabFromCurrentWindowIdSpy.mockResolvedValue(sender.tab);
+        tabsSendMessageSpy.mockImplementation();
+      });
+
+      it("opens the autofill inline menu by sending a message to the current tab", async () => {
+        sendMockExtensionMessage({ command: "openAutofillInlineMenu" }, sender);
+        await flushPromises();
+
+        expect(tabsSendMessageSpy).toHaveBeenCalledWith(
+          sender.tab,
+          {
+            command: "openAutofillInlineMenu",
+            isFocusingFieldElement: false,
+            isOpeningFullAutofillInlineMenu: false,
+            authStatus: 2,
+          },
+          { frameId: 0 },
+        );
+      });
+
+      it("sends the open menu message to the focused field's frameId", async () => {
+        sender.frameId = 10;
+        sendMockExtensionMessage({ command: "updateFocusedFieldData" }, sender);
+        await flushPromises();
+
+        sendMockExtensionMessage({ command: "openAutofillInlineMenu" }, sender);
+        await flushPromises();
+
+        expect(tabsSendMessageSpy).toHaveBeenCalledWith(
+          sender.tab,
+          {
+            command: "openAutofillInlineMenu",
+            isFocusingFieldElement: false,
+            isOpeningFullAutofillInlineMenu: false,
+            authStatus: 2,
+          },
+          { frameId: 10 },
+        );
+      });
+    });
+  });
+
+  describe("inline menu button message handlers", () => {});
+
+  describe("inline menu list message handlers", () => {});
 });
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 70ba44aecc..8a519ad5a1 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -49,7 +49,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   private readonly openUnlockPopout = openUnlockPopout;
   private readonly openViewVaultItemPopout = openViewVaultItemPopout;
   private readonly openAddEditVaultItemPopout = openAddEditVaultItemPopout;
-  private overlayLoginCiphers: Map<string, CipherView> = new Map();
+  private inlineMenuCiphers: Map<string, CipherView> = new Map();
   private pageDetailsForTab: PageDetailsForTab = {};
   private subFrameOffsetsForTab: SubFrameOffsetsForTab = {};
   private updateInlineMenuPositionTimeout: number | NodeJS.Timeout;
@@ -67,8 +67,8 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     autofillOverlayElementClosed: ({ message, sender }) =>
       this.overlayElementClosed(message, sender),
     autofillOverlayAddNewVaultItem: ({ message, sender }) => this.addNewVaultItem(message, sender),
-    checkIsOverlayLoginCiphersPopulated: ({ sender }) =>
-      this.checkIsOverlayLoginCiphersPopulated(sender),
+    checkIsInlineMenuCiphersPopulated: ({ sender }) =>
+      this.checkIsInlineMenuCiphersPopulated(sender),
     updateFocusedFieldData: ({ message, sender }) => this.setFocusedFieldData(message, sender),
     updateIsFieldCurrentlyFocused: ({ message }) => this.updateIsFieldCurrentlyFocused(message),
     checkIsFieldCurrentlyFocused: () => this.checkIsFieldCurrentlyFocused(),
@@ -179,12 +179,12 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       return;
     }
 
-    this.overlayLoginCiphers = new Map();
+    this.inlineMenuCiphers = new Map();
     const ciphersViews = (await this.cipherService.getAllDecryptedForUrl(currentTab.url)).sort(
       (a, b) => this.cipherService.sortCiphersByLastUsedThenName(a, b),
     );
     for (let cipherIndex = 0; cipherIndex < ciphersViews.length; cipherIndex++) {
-      this.overlayLoginCiphers.set(`overlay-cipher-${cipherIndex}`, ciphersViews[cipherIndex]);
+      this.inlineMenuCiphers.set(`overlay-cipher-${cipherIndex}`, ciphersViews[cipherIndex]);
     }
 
     const ciphers = await this.getOverlayCipherData();
@@ -200,7 +200,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
    */
   private async getOverlayCipherData(): Promise<OverlayCipherData[]> {
     const showFavicons = await firstValueFrom(this.domainSettingsService.showFavicons$);
-    const overlayCiphersArray = Array.from(this.overlayLoginCiphers);
+    const overlayCiphersArray = Array.from(this.inlineMenuCiphers);
     const overlayCipherData: OverlayCipherData[] = [];
 
     for (let cipherIndex = 0; cipherIndex < overlayCiphersArray.length; cipherIndex++) {
@@ -388,7 +388,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     );
     if (
       mostRecentlyFocusedFieldHasValue &&
-      (this.checkIsOverlayLoginCiphersPopulated(sender) ||
+      (this.checkIsInlineMenuCiphersPopulated(sender) ||
         (await this.getAuthStatus()) !== AuthenticationStatus.Unlocked)
     ) {
       return;
@@ -401,7 +401,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
    * Triggers autofill for the selected cipher in the inline menu list. Also places
    * the selected cipher at the top of the list of ciphers.
    *
-   * @param overlayCipherId - Cipher ID corresponding to the overlayLoginCiphers map. Does not correspond to the actual cipher's ID.
+   * @param overlayCipherId - Cipher ID corresponding to the inlineMenuCiphers map. Does not correspond to the actual cipher's ID.
    * @param sender - The sender of the port message
    */
   private async fillSelectedInlineMenuListItem(
@@ -413,7 +413,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       return;
     }
 
-    const cipher = this.overlayLoginCiphers.get(overlayCipherId);
+    const cipher = this.inlineMenuCiphers.get(overlayCipherId);
 
     if (await this.autofillService.isPasswordRepromptRequired(cipher, sender.tab)) {
       return;
@@ -430,7 +430,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       this.platformUtilsService.copyToClipboard(totpCode);
     }
 
-    this.overlayLoginCiphers = new Map([[overlayCipherId, cipher], ...this.overlayLoginCiphers]);
+    this.inlineMenuCiphers = new Map([[overlayCipherId, cipher], ...this.inlineMenuCiphers]);
   }
 
   /**
@@ -801,14 +801,14 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   /**
    * Triggers the opening of a vault item popout window associated
    * with the passed cipher ID.
-   * @param overlayCipherId - Cipher ID corresponding to the overlayLoginCiphers map. Does not correspond to the actual cipher's ID.
+   * @param overlayCipherId - Cipher ID corresponding to the inlineMenuCiphers map. Does not correspond to the actual cipher's ID.
    * @param sender - The sender of the port message
    */
   private async viewSelectedCipher(
     { overlayCipherId }: OverlayPortMessage,
     { sender }: chrome.runtime.Port,
   ) {
-    const cipher = this.overlayLoginCiphers.get(overlayCipherId);
+    const cipher = this.inlineMenuCiphers.get(overlayCipherId);
     if (!cipher) {
       return;
     }
@@ -945,18 +945,34 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     await BrowserApi.sendMessage("inlineAutofillMenuRefreshAddEditCipher");
   }
 
+  /**
+   * 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
+   */
   private updateIsFieldCurrentlyFocused(message: OverlayBackgroundExtensionMessage) {
     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.
+   *
+   * @param message - The message received from the web page
+   */
   private updateIsFieldCurrentlyFilling(message: OverlayBackgroundExtensionMessage) {
     this.isFieldCurrentlyFilling = message.isFieldCurrentlyFilling;
   }
 
+  /**
+   * Allows a content script to check if a form field is currently being autofilled.
+   */
   private checkIsFieldCurrentlyFilling() {
     return this.isFieldCurrentlyFilling;
   }
@@ -977,8 +993,8 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     );
   }
 
-  private checkIsOverlayLoginCiphersPopulated(sender: chrome.runtime.MessageSender) {
-    return sender.tab.id === this.focusedFieldData.tabId && this.overlayLoginCiphers.size > 0;
+  private checkIsInlineMenuCiphersPopulated(sender: chrome.runtime.MessageSender) {
+    return sender.tab.id === this.focusedFieldData.tabId && this.inlineMenuCiphers.size > 0;
   }
 
   private updateInlineMenuButtonColorScheme() {
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 d9b574260c..b5b5075b59 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
@@ -18,7 +18,7 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
   private ariaAlertTimeout: number | NodeJS.Timeout;
   private delayedCloseTimeout: number | NodeJS.Timeout;
   private readonly fadeInOpacityTransition = "opacity 125ms ease-out 0s";
-  private readonly fadeOutOpacityTransition = "opacity 75ms ease-in 0s";
+  private readonly fadeOutOpacityTransition = "opacity 60ms ease-out 0s";
   private iframeStyles: Partial<CSSStyleDeclaration> = {
     all: "initial",
     position: "fixed",
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 305bb76441..d23faf3fab 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -1022,7 +1022,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
   }
 
   private async isInlineMenuCiphersPopulated() {
-    return (await this.sendExtensionMessage("checkIsOverlayLoginCiphersPopulated")) === true;
+    return (await this.sendExtensionMessage("checkIsInlineMenuCiphersPopulated")) === true;
   }
 
   /**