diff --git a/change/@fluentui-react-popover-ea9e0418-25e8-45e1-8dda-ffbe8169164a.json b/change/@fluentui-react-popover-ea9e0418-25e8-45e1-8dda-ffbe8169164a.json
new file mode 100644
index 0000000000000..2901078e0ee16
--- /dev/null
+++ b/change/@fluentui-react-popover-ea9e0418-25e8-45e1-8dda-ffbe8169164a.json
@@ -0,0 +1,7 @@
+{
+  "type": "patch",
+  "comment": "fix: close Popover when focus escapes outside while trapFocus is enabled",
+  "packageName": "@fluentui/react-popover",
+  "email": "petrduda@microsoft.com",
+  "dependentChangeType": "patch"
+}
diff --git a/packages/react-components/react-popover/library/etc/react-popover.api.md b/packages/react-components/react-popover/library/etc/react-popover.api.md
index 239f1482b6e14..3a82e29fd5a73 100644
--- a/packages/react-components/react-popover/library/etc/react-popover.api.md
+++ b/packages/react-components/react-popover/library/etc/react-popover.api.md
@@ -33,7 +33,7 @@ export type OnOpenChangeData = {
 };
 
 // @public
-export type OpenPopoverEvents = MouseEvent | TouchEvent | React_2.FocusEvent<HTMLElement> | React_2.KeyboardEvent<HTMLElement> | React_2.MouseEvent<HTMLElement>;
+export type OpenPopoverEvents = MouseEvent | TouchEvent | FocusEvent | React_2.FocusEvent<HTMLElement> | React_2.KeyboardEvent<HTMLElement> | React_2.MouseEvent<HTMLElement>;
 
 // @public
 export const Popover: React_2.FC<PopoverProps>;
diff --git a/packages/react-components/react-popover/library/src/components/Popover/Popover.cy.tsx b/packages/react-components/react-popover/library/src/components/Popover/Popover.cy.tsx
index 39ee679ee7990..6a0d888e9c597 100644
--- a/packages/react-components/react-popover/library/src/components/Popover/Popover.cy.tsx
+++ b/packages/react-components/react-popover/library/src/components/Popover/Popover.cy.tsx
@@ -453,6 +453,108 @@ describe('Popover', () => {
         cy.contains('Two').should('have.focus');
       });
     });
+
+    describe('close on focus escape', () => {
+      it('should close when focus is programmatically moved outside', () => {
+        mount(
+          <>
+            <button id="outside">Outside</button>
+            <Popover trapFocus>
+              <PopoverTrigger disableButtonEnhancement>
+                <button>Popover trigger</button>
+              </PopoverTrigger>
+              <PopoverSurface>
+                <button>Inside</button>
+              </PopoverSurface>
+            </Popover>
+          </>,
+        );
+
+        cy.get(popoverTriggerSelector).click();
+        cy.get(popoverInteractiveContentSelector).should('be.visible');
+        cy.get('#outside').focus();
+        cy.get(popoverInteractiveContentSelector).should('not.exist');
+      });
+
+      it('should close with inertTrapFocus when focus is programmatically moved outside', () => {
+        mount(
+          <>
+            <button id="outside">Outside</button>
+            <Popover trapFocus inertTrapFocus>
+              <PopoverTrigger disableButtonEnhancement>
+                <button>Popover trigger</button>
+              </PopoverTrigger>
+              <PopoverSurface>
+                <button>Inside</button>
+              </PopoverSurface>
+            </Popover>
+          </>,
+        );
+
+        cy.get(popoverTriggerSelector).click();
+        cy.get(popoverInteractiveContentSelector).should('be.visible');
+        cy.get('#outside').focus();
+        cy.get(popoverInteractiveContentSelector).should('not.exist');
+      });
+
+      it('should not close without trapFocus when focus moves outside', () => {
+        mount(
+          <>
+            <button id="outside">Outside</button>
+            <Popover>
+              <PopoverTrigger disableButtonEnhancement>
+                <button>Popover trigger</button>
+              </PopoverTrigger>
+              <PopoverSurface>This is a popover</PopoverSurface>
+            </Popover>
+          </>,
+        );
+
+        cy.get(popoverTriggerSelector).click();
+        cy.get(popoverContentSelector).should('be.visible');
+        cy.get('#outside').focus();
+        cy.get(popoverContentSelector).should('be.visible');
+      });
+
+      it('should not close when closeOnFocusOutside is false', () => {
+        mount(
+          <>
+            <button id="outside">Outside</button>
+            <Popover trapFocus {...({ closeOnFocusOutside: false } as unknown as PopoverProps)}>
+              <PopoverTrigger disableButtonEnhancement>
+                <button>Popover trigger</button>
+              </PopoverTrigger>
+              <PopoverSurface>
+                <button>Inside</button>
+              </PopoverSurface>
+            </Popover>
+          </>,
+        );
+
+        cy.get(popoverTriggerSelector).click();
+        cy.get(popoverInteractiveContentSelector).should('be.visible');
+        cy.get('#outside').focus();
+        cy.get(popoverInteractiveContentSelector).should('be.visible');
+      });
+
+      it('should not close when focus moves to the trigger', () => {
+        mount(
+          <Popover trapFocus>
+            <PopoverTrigger disableButtonEnhancement>
+              <button>Popover trigger</button>
+            </PopoverTrigger>
+            <PopoverSurface>
+              <button>Inside</button>
+            </PopoverSurface>
+          </Popover>,
+        );
+
+        cy.get(popoverTriggerSelector).click();
+        cy.get(popoverInteractiveContentSelector).should('be.visible');
+        cy.get(popoverTriggerSelector).focus();
+        cy.get(popoverInteractiveContentSelector).should('be.visible');
+      });
+    });
   });
 
   describe('with Iframe', () => {
diff --git a/packages/react-components/react-popover/library/src/components/Popover/Popover.test.tsx b/packages/react-components/react-popover/library/src/components/Popover/Popover.test.tsx
index 7a5c20e00b508..b6339053a9f9c 100644
--- a/packages/react-components/react-popover/library/src/components/Popover/Popover.test.tsx
+++ b/packages/react-components/react-popover/library/src/components/Popover/Popover.test.tsx
@@ -1,8 +1,9 @@
 import * as React from 'react';
 import { Popover } from './Popover';
-import { renderHook } from '@testing-library/react-hooks';
+import { renderHook, act } from '@testing-library/react-hooks';
 import { usePopover_unstable } from './usePopover';
 import { isConformant } from '../../testing/isConformant';
+import type { PopoverProps } from './Popover.types';
 
 describe('Popover', () => {
   isConformant({
@@ -37,4 +38,182 @@ describe('Popover', () => {
     // Assert
     expect(result.current.withArrow).toBe(false);
   });
+
+  describe('close on focus outside', () => {
+    it('should close when trapFocus is enabled and focus moves outside', () => {
+      const onOpenChange = jest.fn();
+      const outsideButton = document.createElement('button');
+      const popoverContent = document.createElement('div');
+      document.body.appendChild(outsideButton);
+      document.body.appendChild(popoverContent);
+
+      const { result } = renderHook(
+        ({ open }) =>
+          usePopover_unstable({
+            open,
+            trapFocus: true,
+            onOpenChange,
+            children: <div />,
+          }),
+        { initialProps: { open: true } },
+      );
+
+      // Set the contentRef to simulate mounted popover content
+      act(() => {
+        (result.current.contentRef as React.RefObject<HTMLElement | null>).current = popoverContent;
+      });
+
+      act(() => {
+        outsideButton.dispatchEvent(new FocusEvent('focusin', { bubbles: true }));
+      });
+
+      expect(onOpenChange).toHaveBeenCalledWith(expect.anything(), { open: false });
+
+      document.body.removeChild(outsideButton);
+      document.body.removeChild(popoverContent);
+    });
+
+    it('should not close when trapFocus is not enabled and focus moves outside', () => {
+      const onOpenChange = jest.fn();
+      const outsideButton = document.createElement('button');
+      document.body.appendChild(outsideButton);
+
+      renderHook(() =>
+        usePopover_unstable({
+          open: true,
+          trapFocus: false,
+          onOpenChange,
+          children: <div />,
+        }),
+      );
+
+      act(() => {
+        outsideButton.dispatchEvent(new FocusEvent('focusin', { bubbles: true }));
+      });
+
+      expect(onOpenChange).not.toHaveBeenCalled();
+
+      document.body.removeChild(outsideButton);
+    });
+
+    it('should not close when popover is not open', () => {
+      const onOpenChange = jest.fn();
+      const outsideButton = document.createElement('button');
+      document.body.appendChild(outsideButton);
+
+      renderHook(() =>
+        usePopover_unstable({
+          open: false,
+          trapFocus: true,
+          onOpenChange,
+          children: <div />,
+        }),
+      );
+
+      act(() => {
+        outsideButton.dispatchEvent(new FocusEvent('focusin', { bubbles: true }));
+      });
+
+      expect(onOpenChange).not.toHaveBeenCalled();
+
+      document.body.removeChild(outsideButton);
+    });
+
+    it('should also close when inertTrapFocus is enabled and focus moves to a page element outside', () => {
+      const onOpenChange = jest.fn();
+      const outsideButton = document.createElement('button');
+      const popoverContent = document.createElement('div');
+      document.body.appendChild(outsideButton);
+      document.body.appendChild(popoverContent);
+
+      const { result } = renderHook(() =>
+        usePopover_unstable({
+          open: true,
+          trapFocus: true,
+          inertTrapFocus: true,
+          onOpenChange,
+          children: <div />,
+        }),
+      );
+
+      act(() => {
+        (result.current.contentRef as React.RefObject<HTMLElement | null>).current = popoverContent;
+      });
+
+      act(() => {
+        outsideButton.dispatchEvent(new FocusEvent('focusin', { bubbles: true }));
+      });
+
+      expect(onOpenChange).toHaveBeenCalledWith(expect.anything(), { open: false });
+
+      document.body.removeChild(outsideButton);
+      document.body.removeChild(popoverContent);
+    });
+
+    it('should not close when closeOnFocusOutside is false', () => {
+      const onOpenChange = jest.fn();
+      const outsideButton = document.createElement('button');
+      const popoverContent = document.createElement('div');
+      document.body.appendChild(outsideButton);
+      document.body.appendChild(popoverContent);
+
+      const { result } = renderHook(
+        ({ open }) =>
+          usePopover_unstable({
+            open,
+            trapFocus: true,
+            closeOnFocusOutside: false,
+            onOpenChange,
+            children: <div />,
+          } as unknown as PopoverProps),
+        { initialProps: { open: true } },
+      );
+
+      act(() => {
+        (result.current.contentRef as React.RefObject<HTMLElement | null>).current = popoverContent;
+      });
+
+      act(() => {
+        outsideButton.dispatchEvent(new FocusEvent('focusin', { bubbles: true }));
+      });
+
+      expect(onOpenChange).not.toHaveBeenCalled();
+
+      document.body.removeChild(outsideButton);
+      document.body.removeChild(popoverContent);
+    });
+
+    it('should not close when focus moves to the trigger element', () => {
+      const onOpenChange = jest.fn();
+      const triggerButton = document.createElement('button');
+      const popoverContent = document.createElement('div');
+      document.body.appendChild(triggerButton);
+      document.body.appendChild(popoverContent);
+
+      const { result } = renderHook(
+        ({ open }) =>
+          usePopover_unstable({
+            open,
+            trapFocus: true,
+            onOpenChange,
+            children: <div />,
+          }),
+        { initialProps: { open: true } },
+      );
+
+      act(() => {
+        (result.current.contentRef as React.RefObject<HTMLElement | null>).current = popoverContent;
+        (result.current.triggerRef as React.RefObject<HTMLElement | null>).current = triggerButton;
+      });
+
+      act(() => {
+        triggerButton.dispatchEvent(new FocusEvent('focusin', { bubbles: true }));
+      });
+
+      expect(onOpenChange).not.toHaveBeenCalled();
+
+      document.body.removeChild(triggerButton);
+      document.body.removeChild(popoverContent);
+    });
+  });
 });
diff --git a/packages/react-components/react-popover/library/src/components/Popover/Popover.types.ts b/packages/react-components/react-popover/library/src/components/Popover/Popover.types.ts
index 251eff842d04d..cac9e90d6d36e 100644
--- a/packages/react-components/react-popover/library/src/components/Popover/Popover.types.ts
+++ b/packages/react-components/react-popover/library/src/components/Popover/Popover.types.ts
@@ -236,6 +236,7 @@ export type OnOpenChangeData = { open: boolean };
 export type OpenPopoverEvents =
   | MouseEvent
   | TouchEvent
+  | FocusEvent
   | React.FocusEvent<HTMLElement>
   | React.KeyboardEvent<HTMLElement>
   | React.MouseEvent<HTMLElement>;
diff --git a/packages/react-components/react-popover/library/src/components/Popover/usePopover.ts b/packages/react-components/react-popover/library/src/components/Popover/usePopover.ts
index 265425dbad100..a19e11fbc1848 100644
--- a/packages/react-components/react-popover/library/src/components/Popover/usePopover.ts
+++ b/packages/react-components/react-popover/library/src/components/Popover/usePopover.ts
@@ -168,6 +168,39 @@ export const usePopoverBase_unstable = (props: PopoverBaseProps): PopoverBaseSta
     disabled: !open || !closeOnScroll,
   });
 
+  // When trapFocus is enabled, close the popover if focus is programmatically moved outside
+  // (e.g. via element.focus()), which doesn't trigger click or scroll dismiss handlers.
+  // Internal `closeOnFocusOutside` prop allows consumers to opt out during gradual rollout.
+  const closeOnFocusOutside =
+    (props as PopoverBaseProps & { closeOnFocusOutside?: boolean }).closeOnFocusOutside ?? true;
+
+  const closeOnFocusOutCallback = useEventCallback((ev: FocusEvent) => {
+    const target = (ev.composedPath()[0] ?? ev.target) as HTMLElement;
+    const contentElement = positioningRefs.contentRef.current;
+    const triggerElement = positioningRefs.triggerRef.current ?? null;
+
+    if (!contentElement) {
+      return;
+    }
+
+    const isOutside = !elementContains(contentElement, target) && !elementContains(triggerElement, target);
+
+    if (isOutside) {
+      setOpen(ev, false);
+    }
+  });
+
+  React.useEffect(() => {
+    if (!open || !props.trapFocus || !closeOnFocusOutside) {
+      return;
+    }
+
+    targetDocument?.addEventListener('focusin', closeOnFocusOutCallback, true);
+    return () => {
+      targetDocument?.removeEventListener('focusin', closeOnFocusOutCallback, true);
+    };
+  }, [open, props.trapFocus, closeOnFocusOutside, targetDocument, closeOnFocusOutCallback]);
+
   const { findFirstFocusable } = useFocusFinders();
   const activateModal = useActivateModal();