diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index c52bceec72..f08176469c 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -131,8 +131,7 @@ export type PortOnMessageHandlerParams = PortMessageParam & PortConnectionParam;
 export type InlineMenuButtonPortMessageHandlers = {
   [key: string]: CallableFunction;
   autofillInlineMenuButtonClicked: ({ port }: PortConnectionParam) => void;
-  closeAutofillInlineMenu: ({ port }: PortConnectionParam) => void;
-  forceCloseAutofillInlineMenu: ({ port }: PortConnectionParam) => void;
+  triggerDelayedInlineMenuClosure: ({ port }: PortConnectionParam) => void;
   autofillInlineMenuBlurred: () => void;
   redirectAutofillInlineMenuFocusOut: ({ message, port }: PortOnMessageHandlerParams) => void;
   updateAutofillInlineMenuColorScheme: () => void;
@@ -141,7 +140,6 @@ export type InlineMenuButtonPortMessageHandlers = {
 export type InlineMenuListPortMessageHandlers = {
   [key: string]: CallableFunction;
   checkAutofillInlineMenuButtonFocused: () => void;
-  forceCloseAutofillInlineMenu: ({ port }: PortConnectionParam) => void;
   autofillInlineMenuBlurred: () => void;
   unlockVault: ({ port }: PortConnectionParam) => void;
   fillSelectedAutofillInlineMenuListItem: ({ message, port }: PortOnMessageHandlerParams) => void;
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index 6190861851..70ba44aecc 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -96,9 +96,8 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   };
   private readonly inlineMenuButtonPortMessageHandlers: InlineMenuButtonPortMessageHandlers = {
     autofillInlineMenuButtonClicked: ({ port }) => this.handleInlineMenuButtonClicked(port),
-    closeAutofillInlineMenu: ({ port }) => this.closeInlineMenu(port.sender),
-    forceCloseAutofillInlineMenu: ({ port }) =>
-      this.closeInlineMenu(port.sender, { forceCloseAutofillInlineMenu: true }),
+    triggerDelayedInlineMenuClosure: ({ port }) =>
+      this.triggerDelayedInlineMenuClosure(port.sender),
     autofillInlineMenuBlurred: () => this.checkInlineMenuListFocused(),
     redirectAutofillInlineMenuFocusOut: ({ message, port }) =>
       this.redirectInlineMenuFocusOut(message, port),
@@ -106,8 +105,6 @@ export class OverlayBackground implements OverlayBackgroundInterface {
   };
   private readonly inlineMenuListPortMessageHandlers: InlineMenuListPortMessageHandlers = {
     checkAutofillInlineMenuButtonFocused: () => this.checkInlineMenuButtonFocused(),
-    forceCloseAutofillInlineMenu: ({ port }) =>
-      this.closeInlineMenu(port.sender, { forceCloseAutofillInlineMenu: true }),
     autofillInlineMenuBlurred: () => this.checkInlineMenuButtonFocused(),
     unlockVault: ({ port }) => this.unlockVault(port),
     fillSelectedAutofillInlineMenuListItem: ({ message, port }) =>
@@ -510,6 +507,16 @@ export class OverlayBackground implements OverlayBackgroundInterface {
     );
   }
 
+  private triggerDelayedInlineMenuClosure(sender: chrome.runtime.MessageSender) {
+    if (this.isFieldCurrentlyFocused) {
+      return;
+    }
+
+    const message = { command: "triggerDelayedAutofillInlineMenuClosure" };
+    this.inlineMenuButtonPort?.postMessage(message);
+    this.inlineMenuListPort?.postMessage(message);
+  }
+
   /**
    * Handles cleanup when an overlay element is closed. Disconnects
    * the list and button ports and sets them to null.
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 efab7cba6f..3204727f0d 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
@@ -16,6 +16,8 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
   private iframe: HTMLIFrameElement;
   private ariaAlertElement: HTMLDivElement;
   private ariaAlertTimeout: number | NodeJS.Timeout;
+  private delayedCloseTimeout: number | NodeJS.Timeout;
+  private readonly defaultOpacityTransition = "opacity 125ms ease-out 0s";
   private iframeStyles: Partial<CSSStyleDeclaration> = {
     all: "initial",
     position: "fixed",
@@ -23,7 +25,7 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
     zIndex: "2147483647",
     lineHeight: "0",
     overflow: "hidden",
-    transition: "opacity 125ms ease-out 0s",
+    transition: this.defaultOpacityTransition,
     visibility: "visible",
     clipPath: "none",
     pointerEvents: "auto",
@@ -47,6 +49,7 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
     updateInlineMenuIframePosition: ({ message }) => this.updateIframePosition(message.styles),
     updateInlineMenuHidden: ({ message }) => this.updateElementStyles(this.iframe, message.styles),
     updateAutofillInlineMenuColorScheme: () => this.updateAutofillInlineMenuColorScheme(),
+    triggerDelayedAutofillInlineMenuClosure: () => this.handleDelayedAutofillInlineMenuClosure(),
   };
 
   constructor(
@@ -403,4 +406,24 @@ export class AutofillInlineMenuIframeService implements AutofillInlineMenuIframe
 
     return false;
   }
+
+  private handleDelayedAutofillInlineMenuClosure() {
+    if (this.delayedCloseTimeout) {
+      clearTimeout(this.delayedCloseTimeout);
+    }
+
+    this.updateElementStyles(this.iframe, {
+      opacity: "0",
+      transition: "none",
+      pointerEvents: "none",
+    });
+
+    this.delayedCloseTimeout = globalThis.setTimeout(() => {
+      this.updateElementStyles(this.iframe, {
+        transition: this.defaultOpacityTransition,
+        pointerEvents: "auto",
+      });
+      this.forceCloseAutofillInlineMenu();
+    }, 250);
+  }
 }
diff --git a/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.spec.ts b/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.spec.ts
index 23424f189b..28f2a3ca19 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.spec.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.spec.ts
@@ -74,7 +74,7 @@ describe("AutofillInlineMenuButton", () => {
       await flushPromises();
 
       expect(globalThis.parent.postMessage).not.toHaveBeenCalledWith({
-        command: "closeAutofillInlineMenu",
+        command: "triggerDelayedInlineMenuClosure",
       });
     });
 
@@ -85,7 +85,7 @@ describe("AutofillInlineMenuButton", () => {
       await flushPromises();
 
       expect(globalThis.parent.postMessage).toHaveBeenCalledWith(
-        { command: "closeAutofillInlineMenu", portKey },
+        { command: "triggerDelayedInlineMenuClosure", portKey },
         "*",
       );
     });
diff --git a/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.ts b/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.ts
index 03debe861c..29bdce7b97 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/pages/button/autofill-inline-menu-button.ts
@@ -121,7 +121,7 @@ class AutofillInlineMenuButton extends AutofillInlineMenuPageElement {
       return;
     }
 
-    this.postMessageToParent({ command: "closeAutofillInlineMenu" });
+    this.postMessageToParent({ command: "triggerDelayedInlineMenuClosure" });
   }
 }
 
diff --git a/apps/browser/src/autofill/overlay/inline-menu/pages/menu-container/autofill-inline-menu-container.ts b/apps/browser/src/autofill/overlay/inline-menu/pages/menu-container/autofill-inline-menu-container.ts
index a516dedd46..7e5a7ba35c 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/pages/menu-container/autofill-inline-menu-container.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/pages/menu-container/autofill-inline-menu-container.ts
@@ -69,8 +69,6 @@ export class AutofillInlineMenuContainer {
 
   private setupPortMessageListener = (message: InitInlineMenuElementMessage) => {
     this.port = chrome.runtime.connect({ name: this.portName });
-    this.port.onMessage.addListener(this.handlePortMessage);
-
     this.postMessageToInlineMenuPage(message);
   };
 
@@ -90,14 +88,6 @@ export class AutofillInlineMenuContainer {
     this.port.postMessage(message);
   }
 
-  private handlePortMessage = (message: any, port: chrome.runtime.Port) => {
-    if (port.name !== this.portName) {
-      return;
-    }
-
-    this.postMessageToInlineMenuPage(message);
-  };
-
   private handleWindowMessage = (event: MessageEvent) => {
     const message = event.data;
     if (this.isForeignWindowMessage(event)) {