diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index c88e25b5aa..719e5603ad 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -54,6 +54,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   private pageDetailsForTab: PageDetailsForTab = {};
   private subFrameOffsetsForTab: SubFrameOffsetsForTab = {};
   private updateInlineMenuPositionTimeout: number | NodeJS.Timeout;
+  private inlineMenuFadeInTimeout: number | NodeJS.Timeout;
   private userAuthStatus: AuthenticationStatus = AuthenticationStatus.LoggedOut;
   private inlineMenuButtonPort: chrome.runtime.Port;
   private inlineMenuListPort: chrome.runtime.Port;
@@ -440,7 +441,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       return;
     }
 
-    if (sender.frameId === this.focusedFieldData?.frameId && this.isFieldCurrentlyFocused) {
+    if (this.isFieldCurrentlyFocused) {
       return;
     }
 
@@ -518,9 +519,11 @@ export class OverlayBackground implements OverlayBackgroundInterface {
       subFrameOffsets = subFrameOffsetsForTab.get(this.focusedFieldData.frameId);
     }
 
+    this.setInlineMenuFadeInTimeout();
+
     if (overlayElement === AutofillOverlayElement.Button) {
       this.inlineMenuButtonPort?.postMessage({
-        command: "updateIframePosition",
+        command: "updateInlineMenuIframePosition",
         styles: this.getInlineMenuButtonPosition(subFrameOffsets),
       });
 
@@ -528,11 +531,23 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     }
 
     this.inlineMenuListPort?.postMessage({
-      command: "updateIframePosition",
+      command: "updateInlineMenuIframePosition",
       styles: this.getInlineMenuListPosition(subFrameOffsets),
     });
   }
 
+  private setInlineMenuFadeInTimeout() {
+    if (this.inlineMenuFadeInTimeout) {
+      globalThis.clearTimeout(this.inlineMenuFadeInTimeout);
+    }
+
+    const message = { command: "updateInlineMenuIframePosition", styles: { opacity: "1" } };
+    this.inlineMenuFadeInTimeout = globalThis.setTimeout(() => {
+      this.inlineMenuButtonPort?.postMessage(message);
+      this.inlineMenuListPort?.postMessage(message);
+    }, 75);
+  }
+
   /**
    * Gets the position of the focused field and calculates the position
    * of the inline menu button based on the focused field's position and dimensions.
@@ -600,6 +615,14 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     { focusedFieldData }: OverlayBackgroundExtensionMessage,
     sender: chrome.runtime.MessageSender,
   ) {
+    if (this.focusedFieldData?.frameId && this.focusedFieldData.frameId !== sender.frameId) {
+      void BrowserApi.tabSendMessage(
+        sender.tab,
+        { command: "unsetMostRecentlyFocusedField" },
+        { frameId: this.focusedFieldData.frameId },
+      );
+    }
+
     this.focusedFieldData = { ...focusedFieldData, tabId: sender.tab.id, frameId: sender.frameId };
   }
 
@@ -922,7 +945,7 @@ export class OverlayBackground implements OverlayBackgroundInterface {
 
   private updateInlineMenuListHeight(message: OverlayBackgroundExtensionMessage) {
     this.inlineMenuListPort?.postMessage({
-      command: "updateIframePosition",
+      command: "updateInlineMenuIframePosition",
       styles: message.styles,
     });
   }
diff --git a/apps/browser/src/autofill/overlay/inline-menu/abstractions/autofill-inline-menu-iframe.service.ts b/apps/browser/src/autofill/overlay/inline-menu/abstractions/autofill-inline-menu-iframe.service.ts
index 3914baaf0f..37979a3f43 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/abstractions/autofill-inline-menu-iframe.service.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/abstractions/autofill-inline-menu-iframe.service.ts
@@ -15,7 +15,9 @@ export type BackgroundPortMessageHandlers = {
     message,
   }: AutofillInlineMenuIframeExtensionMessageParam) => void;
   initAutofillInlineMenuList: ({ message }: AutofillInlineMenuIframeExtensionMessageParam) => void;
-  updateIframePosition: ({ message }: AutofillInlineMenuIframeExtensionMessageParam) => void;
+  updateInlineMenuIframePosition: ({
+    message,
+  }: AutofillInlineMenuIframeExtensionMessageParam) => void;
   updateInlineMenuHidden: ({ message }: AutofillInlineMenuIframeExtensionMessageParam) => void;
   updateAutofillInlineMenuColorScheme: () => void;
 };
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 193f4052c4..398fac8f33 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
@@ -104,9 +104,7 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
     }
 
     this.buttonElement.remove();
-
     this.isButtonVisible = false;
-
     void this.sendExtensionMessage("autofillOverlayElementClosed", {
       overlayElement: AutofillOverlayElement.Button,
     });
@@ -121,9 +119,7 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
     }
 
     this.listElement.remove();
-
     this.isListVisible = false;
-
     void this.sendExtensionMessage("autofillOverlayElementClosed", {
       overlayElement: AutofillOverlayElement.List,
     });
diff --git a/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.spec.ts b/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.spec.ts
index dc39d6e9de..e0610bd148 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.spec.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/iframe-content/autofill-inline-menu-iframe.service.spec.ts
@@ -193,9 +193,9 @@ describe("AutofillInlineMenuIframeService", () => {
       });
 
       it("handles port messages that are registered with the message handlers and does not pass the message on to the iframe", () => {
-        jest.spyOn(autofillInlineMenuIframeService as any, "updateIframePosition");
+        jest.spyOn(autofillInlineMenuIframeService as any, "updateInlineMenuIframePosition");
 
-        sendPortMessage(portSpy, { command: "updateIframePosition" });
+        sendPortMessage(portSpy, { command: "updateInlineMenuIframePosition" });
 
         expect(
           autofillInlineMenuIframeService["iframe"].contentWindow.postMessage,
@@ -344,7 +344,7 @@ describe("AutofillInlineMenuIframeService", () => {
           jest.spyOn(globalThis.document, "hasFocus").mockReturnValue(false);
 
           sendPortMessage(portSpy, {
-            command: "updateIframePosition",
+            command: "updateInlineMenuIframePosition",
             styles: { top: 100, left: 100 },
           });
 
@@ -355,7 +355,7 @@ describe("AutofillInlineMenuIframeService", () => {
           const styles = { top: "100px", left: "100px" };
 
           sendPortMessage(portSpy, {
-            command: "updateIframePosition",
+            command: "updateInlineMenuIframePosition",
             styles,
           });
 
@@ -368,7 +368,7 @@ describe("AutofillInlineMenuIframeService", () => {
           const styles = { top: "100px", left: "100px" };
 
           sendPortMessage(portSpy, {
-            command: "updateIframePosition",
+            command: "updateInlineMenuIframePosition",
             styles,
           });
 
@@ -382,7 +382,7 @@ describe("AutofillInlineMenuIframeService", () => {
           const styles = { top: "100px", left: "100px" };
 
           sendPortMessage(portSpy, {
-            command: "updateIframePosition",
+            command: "updateInlineMenuIframePosition",
             styles,
           });
 
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 cb595a456f..af551ad388 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
@@ -44,7 +44,7 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
   private readonly backgroundPortMessageHandlers: BackgroundPortMessageHandlers = {
     initAutofillInlineMenuButton: ({ message }) => this.initAutofillInlineMenu(message),
     initAutofillInlineMenuList: ({ message }) => this.initAutofillInlineMenu(message),
-    updateIframePosition: ({ message }) => this.updateIframePosition(message.styles),
+    updateInlineMenuIframePosition: ({ message }) => this.updateIframePosition(message.styles),
     updateInlineMenuHidden: ({ message }) => this.updateElementStyles(this.iframe, message.styles),
     updateAutofillInlineMenuColorScheme: () => this.updateAutofillInlineMenuColorScheme(),
   };
@@ -248,7 +248,7 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
     }
 
     this.updateElementStyles(this.iframe, position);
-    setTimeout(() => this.updateElementStyles(this.iframe, { opacity: "1" }), 0);
+    // setTimeout(() => this.updateElementStyles(this.iframe, { opacity: "1" }), 0);
     this.announceAriaAlert();
   }
 
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 897bb2d65d..ce5f1a2448 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
@@ -16,6 +16,7 @@ export type AutofillOverlayContentExtensionMessageHandlers = {
   openAutofillInlineMenu: ({ message }: AutofillExtensionMessageParam) => void;
   addNewVaultItemFromOverlay: () => void;
   blurMostRecentlyFocusedField: () => void;
+  unsetMostRecentlyFocusedField: () => void;
   bgUnlockPopoutOpened: () => void;
   bgVaultItemRepromptPopoutOpened: () => void;
   redirectAutofillInlineMenuFocusOut: ({ message }: AutofillExtensionMessageParam) => void;
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 ff09533b89..b65dcd3cd1 100644
--- a/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
+++ b/apps/browser/src/autofill/services/autofill-overlay-content.service.ts
@@ -44,6 +44,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     openAutofillInlineMenu: ({ message }) => this.openAutofillInlineMenu(message),
     addNewVaultItemFromOverlay: () => this.addNewVaultItem(),
     blurMostRecentlyFocusedField: () => this.blurMostRecentlyFocusedField(),
+    unsetMostRecentlyFocusedField: () => this.unsetMostRecentlyFocusedField(),
     bgUnlockPopoutOpened: () => this.blurMostRecentlyFocusedField(true),
     bgVaultItemRepromptPopoutOpened: () => this.blurMostRecentlyFocusedField(true),
     redirectAutofillInlineMenuFocusOut: ({ message }) =>
@@ -162,6 +163,10 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     }
   }
 
+  unsetMostRecentlyFocusedField() {
+    this.mostRecentlyFocusedField = null;
+  }
+
   /**
    * Formats any found user filled fields for a login cipher and sends a message
    * to the background script to add a new cipher.
@@ -797,7 +802,7 @@ export class AutofillOverlayContentService implements AutofillOverlayContentServ
     await this.updateMostRecentlyFocusedField(this.mostRecentlyFocusedField);
     this.updateAutofillInlineMenuElementsPosition();
     setTimeout(async () => {
-      this.toggleAutofillInlineMenuHidden(false);
+      this.toggleAutofillInlineMenuHidden(false, true);
       if (
         await this.hideAutofillInlineMenuListOnFilledField(
           this.mostRecentlyFocusedField as FillableFormFieldElement,