diff --git a/packages/breadcrumbs/spec/web-component-spec.md b/packages/breadcrumbs/spec/web-component-spec.md
index 27fce0d599c..9529d0b0c4a 100644
--- a/packages/breadcrumbs/spec/web-component-spec.md
+++ b/packages/breadcrumbs/spec/web-component-spec.md
@@ -304,3 +304,7 @@ Two shadow slots with the overflow in shadow DOM between them: `<slot name="root
 **Q: Why does `i18n.moreItems` default to `'More items'` rather than an empty string?**
 
 The `aria-label` on the overflow button must always be present — screen readers announce the button as just "button" otherwise. Defaulting to an empty string leaves the application responsible for setting a meaningful label before the component is reachable to assistive tech, which is a setup step that's easy to miss. Providing `'More items'` as the default matches the convention for other Vaadin components with auto-generated control labels (Menu Bar, Combo Box clear button) and keeps the unlabeled state out of reach. Applications still localize via `i18n = { moreItems: '…' }` exactly as before.
+
+**Q: Why does the overlay's focus indicator only appear on keyboard opens?**
+
+The container calls `_focus(idx, { focusVisible: isKeyboardActive() })` when moving focus into the open overlay, matching the convention used by `<vaadin-context-menu>`, `<vaadin-menu-bar>`, `<vaadin-select>`, `<vaadin-app-layout>`, `<vaadin-upload>`, and `<vaadin-master-detail-layout>`. A mouse-driven open is a continuation of a pointer interaction — a focus ring appearing under the user's cursor is visual noise. A keyboard-driven open is the user's only signal that focus has moved into a transient popup, so the ring is essential. `isKeyboardActive()` from `@vaadin/a11y-base` reads the cross-component flag set on every keydown and cleared on every mousedown, so the trigger detection is automatic and consistent with the rest of the library.
diff --git a/packages/breadcrumbs/src/vaadin-breadcrumbs.js b/packages/breadcrumbs/src/vaadin-breadcrumbs.js
index b24610766fb..fd74e1d97de 100644
--- a/packages/breadcrumbs/src/vaadin-breadcrumbs.js
+++ b/packages/breadcrumbs/src/vaadin-breadcrumbs.js
@@ -6,6 +6,7 @@
 import './vaadin-breadcrumbs-item.js';
 import './vaadin-breadcrumbs-overlay.js';
 import { html, LitElement } from 'lit';
+import { isKeyboardActive } from '@vaadin/a11y-base/src/focus-utils.js';
 import { KeyboardDirectionMixin } from '@vaadin/a11y-base/src/keyboard-direction-mixin.js';
 import { defineCustomElement } from '@vaadin/component-base/src/define.js';
 import { ElementMixin } from '@vaadin/component-base/src/element-mixin.js';
@@ -302,7 +303,7 @@ class Breadcrumbs extends KeyboardDirectionMixin(
     // Focus first non-disabled overlay item
     const idx = this._getFocusableIndex();
     if (idx >= 0) {
-      this._focus(idx);
+      this._focus(idx, { focusVisible: isKeyboardActive() });
     }
   }
 
diff --git a/packages/breadcrumbs/test/dom/__snapshots__/breadcrumbs.test.snap.js b/packages/breadcrumbs/test/dom/__snapshots__/breadcrumbs.test.snap.js
index a1fefacd42d..3571d3d4408 100644
--- a/packages/breadcrumbs/test/dom/__snapshots__/breadcrumbs.test.snap.js
+++ b/packages/breadcrumbs/test/dom/__snapshots__/breadcrumbs.test.snap.js
@@ -236,7 +236,6 @@ snapshots["vaadin-breadcrumbs overflow opened"] =
     Home
   </vaadin-breadcrumbs-item>
   <vaadin-breadcrumbs-item
-    focus-ring=""
     focused=""
     path="/docs"
     role="listitem"
diff --git a/packages/breadcrumbs/test/overflow.test.js b/packages/breadcrumbs/test/overflow.test.js
index fdcd0b84d90..34e9278e96b 100644
--- a/packages/breadcrumbs/test/overflow.test.js
+++ b/packages/breadcrumbs/test/overflow.test.js
@@ -1,6 +1,6 @@
 import { expect } from '@vaadin/chai-plugins';
 import { sendKeys } from '@vaadin/test-runner-commands';
-import { fixtureSync, nextRender, nextResize, oneEvent } from '@vaadin/testing-helpers';
+import { fixtureSync, mousedown, nextRender, nextResize, oneEvent } from '@vaadin/testing-helpers';
 import '../vaadin-breadcrumbs.js';
 import { getDeepActiveElement } from '@vaadin/a11y-base/src/focus-utils.js';
 
@@ -187,6 +187,34 @@ describe('overflow', () => {
       const firstItem = breadcrumbs.querySelector('vaadin-breadcrumbs-item[slot="overlay"]');
       expectFocusedItem(firstItem);
     });
+
+    it('should not set focus-ring on the first overlay item when opening via mouse', async () => {
+      mousedown(button);
+      button.click();
+      await oneEvent(overlay, 'vaadin-overlay-open');
+
+      const firstItem = breadcrumbs.querySelector('vaadin-breadcrumbs-item[slot="overlay"]');
+      expectFocusedItem(firstItem);
+      expect(firstItem.hasAttribute('focus-ring')).to.be.false;
+    });
+
+    it('should set focus-ring on the first overlay item when opening via Enter', async () => {
+      button.focus();
+      await sendKeys({ press: 'Enter' });
+      await nextRender();
+
+      const firstItem = breadcrumbs.querySelector('vaadin-breadcrumbs-item[slot="overlay"]');
+      expect(firstItem.hasAttribute('focus-ring')).to.be.true;
+    });
+
+    it('should set focus-ring on the first overlay item when opening via Space', async () => {
+      button.focus();
+      await sendKeys({ press: 'Space' });
+      await nextRender();
+
+      const firstItem = breadcrumbs.querySelector('vaadin-breadcrumbs-item[slot="overlay"]');
+      expect(firstItem.hasAttribute('focus-ring')).to.be.true;
+    });
   });
 
   describe('closing', () => {