diff --git a/.changeset/tabmenu-roving.md b/.changeset/tabmenu-roving.md
new file mode 100644
index 000000000000..f07a41d78a0c
--- /dev/null
+++ b/.changeset/tabmenu-roving.md
@@ -0,0 +1,6 @@
+---
+'@astryxdesign/core': patch
+---
+
+[fix] TabList: the overflow tab menu now uses a roving tabindex — one tab stop with arrow-key navigation between items — instead of making every overflow item a separate tab stop. (#3728)
+@bhamodi
diff --git a/packages/core/src/TabList/TabList.test.tsx b/packages/core/src/TabList/TabList.test.tsx
index b061dda0f481..d26e3b9b39fc 100644
--- a/packages/core/src/TabList/TabList.test.tsx
+++ b/packages/core/src/TabList/TabList.test.tsx
@@ -10,7 +10,7 @@
  */
 
 import {describe, it, expect, vi, beforeAll, afterAll} from 'vitest';
-import {render, screen} from '@testing-library/react';
+import {render, screen, fireEvent} from '@testing-library/react';
 import userEvent from '@testing-library/user-event';
 import {TabList} from './TabList';
 import {Tab} from './Tab';
@@ -702,3 +702,187 @@ describe('TabMenu', () => {
     expect(reportsItem).not.toHaveAttribute('aria-current');
   });
 });
+
+describe('TabMenu keyboard navigation (roving tabindex)', () => {
+  const menuOptions = [
+    {value: 'analytics', label: 'Analytics'},
+    {value: 'reports', label: 'Reports'},
+  ];
+
+  it('exposes the overflow menu as a single Tab stop (one item tabbable, rest -1)', async () => {
+    const user = userEvent.setup();
+    render(
+      <TabList value="home" onChange={() => {}}>
+        <Tab value="home" label="Home" />
+        <TabMenu label="More" options={menuOptions} />
+      </TabList>,
+    );
+
+    await user.click(screen.getByRole('button', {name: /More/}));
+
+    const analytics = screen.getByRole('menuitem', {
+      name: 'Analytics',
+      hidden: true,
+    });
+    const reports = screen.getByRole('menuitem', {
+      name: 'Reports',
+      hidden: true,
+    });
+
+    // Exactly one menu item is in the Tab sequence; arrow keys reach the rest.
+    expect(analytics).toHaveAttribute('tabindex', '0');
+    expect(reports).toHaveAttribute('tabindex', '-1');
+
+    const tabbable = [analytics, reports].filter(
+      el => el.getAttribute('tabindex') === '0',
+    );
+    expect(tabbable).toHaveLength(1);
+  });
+
+  it('moves focus between items with ArrowDown and ArrowUp', async () => {
+    const user = userEvent.setup();
+    render(
+      <TabList value="home" onChange={() => {}}>
+        <Tab value="home" label="Home" />
+        <TabMenu label="More" options={menuOptions} />
+      </TabList>,
+    );
+
+    await user.click(screen.getByRole('button', {name: /More/}));
+    const menu = screen.getByRole('menu', {hidden: true});
+    const analytics = screen.getByRole('menuitem', {
+      name: 'Analytics',
+      hidden: true,
+    });
+    const reports = screen.getByRole('menuitem', {
+      name: 'Reports',
+      hidden: true,
+    });
+
+    fireEvent.keyDown(menu, {key: 'ArrowDown'});
+    expect(analytics).toHaveFocus();
+
+    fireEvent.keyDown(menu, {key: 'ArrowDown'});
+    expect(reports).toHaveFocus();
+
+    fireEvent.keyDown(menu, {key: 'ArrowUp'});
+    expect(analytics).toHaveFocus();
+  });
+
+  it('moves the roving tab stop with arrow navigation', async () => {
+    const user = userEvent.setup();
+    render(
+      <TabList value="home" onChange={() => {}}>
+        <Tab value="home" label="Home" />
+        <TabMenu label="More" options={menuOptions} />
+      </TabList>,
+    );
+
+    await user.click(screen.getByRole('button', {name: /More/}));
+    const menu = screen.getByRole('menu', {hidden: true});
+    const analytics = screen.getByRole('menuitem', {
+      name: 'Analytics',
+      hidden: true,
+    });
+    const reports = screen.getByRole('menuitem', {
+      name: 'Reports',
+      hidden: true,
+    });
+
+    fireEvent.keyDown(menu, {key: 'ArrowDown'}); // focus analytics
+    fireEvent.keyDown(menu, {key: 'ArrowDown'}); // focus reports
+
+    // The tab stop follows focus, so it is still a single stop after moving.
+    expect(reports).toHaveAttribute('tabindex', '0');
+    expect(analytics).toHaveAttribute('tabindex', '-1');
+  });
+
+  it('jumps to first and last item with Home and End', async () => {
+    const user = userEvent.setup();
+    const options = [
+      {value: 'analytics', label: 'Analytics'},
+      {value: 'reports', label: 'Reports'},
+      {value: 'exports', label: 'Exports'},
+    ];
+    render(
+      <TabList value="home" onChange={() => {}}>
+        <Tab value="home" label="Home" />
+        <TabMenu label="More" options={options} />
+      </TabList>,
+    );
+
+    await user.click(screen.getByRole('button', {name: /More/}));
+    const menu = screen.getByRole('menu', {hidden: true});
+    const analytics = screen.getByRole('menuitem', {
+      name: 'Analytics',
+      hidden: true,
+    });
+    const exports = screen.getByRole('menuitem', {
+      name: 'Exports',
+      hidden: true,
+    });
+
+    fireEvent.keyDown(menu, {key: 'End'});
+    expect(exports).toHaveFocus();
+
+    fireEvent.keyDown(menu, {key: 'Home'});
+    expect(analytics).toHaveFocus();
+  });
+
+  it('selects an item with Enter and calls onChange', async () => {
+    const user = userEvent.setup();
+    const handleChange = vi.fn();
+    render(
+      <TabList value="home" onChange={handleChange}>
+        <Tab value="home" label="Home" />
+        <TabMenu label="More" options={menuOptions} />
+      </TabList>,
+    );
+
+    await user.click(screen.getByRole('button', {name: /More/}));
+    const analytics = screen.getByRole('menuitem', {
+      name: 'Analytics',
+      hidden: true,
+    });
+    analytics.focus();
+    fireEvent.keyDown(analytics, {key: 'Enter'});
+
+    expect(handleChange).toHaveBeenCalledWith('analytics');
+  });
+
+  it('closes the menu when Tab is pressed inside it (APG menu-button)', async () => {
+    const user = userEvent.setup();
+    render(
+      <TabList value="home" onChange={() => {}}>
+        <Tab value="home" label="Home" />
+        <TabMenu label="More" options={menuOptions} />
+      </TabList>,
+    );
+
+    await user.click(screen.getByRole('button', {name: /More/}));
+    const menu = screen.getByRole('menu', {hidden: true});
+
+    const hidePopover = vi.mocked(HTMLElement.prototype.hidePopover);
+    hidePopover.mockClear();
+    fireEvent.keyDown(menu, {key: 'Tab'});
+    expect(hidePopover).toHaveBeenCalled();
+  });
+
+  it('closes the menu when Escape is pressed', async () => {
+    const user = userEvent.setup();
+    render(
+      <TabList value="home" onChange={() => {}}>
+        <Tab value="home" label="Home" />
+        <TabMenu label="More" options={menuOptions} />
+      </TabList>,
+    );
+
+    await user.click(screen.getByRole('button', {name: /More/}));
+    const menu = screen.getByRole('menu', {hidden: true});
+
+    const hidePopover = vi.mocked(HTMLElement.prototype.hidePopover);
+    hidePopover.mockClear();
+    fireEvent.keyDown(menu, {key: 'Escape'});
+    expect(hidePopover).toHaveBeenCalled();
+  });
+});
diff --git a/packages/core/src/TabList/TabMenu.tsx b/packages/core/src/TabList/TabMenu.tsx
index 9232037934a4..41fec707722e 100644
--- a/packages/core/src/TabList/TabMenu.tsx
+++ b/packages/core/src/TabList/TabMenu.tsx
@@ -16,7 +16,7 @@
  * - /packages/cli/templates/blocks/components/TabList/ (showcase blocks)
  */
 
-import React, {useCallback, useId, type ReactNode} from 'react';
+import React, {useCallback, useId, useRef, type ReactNode} from 'react';
 import * as stylex from '@stylexjs/stylex';
 import {Icon} from '../Icon';
 import {renderIconSlot, type IconType} from '../Icon';
@@ -262,6 +262,7 @@ export function TabMenu({
 }: TabMenuProps) {
   const tabListCtx = useTabListContext();
   const menuId = useId();
+  const buttonRef = useRef<HTMLButtonElement>(null);
 
   const popover = usePopover({
     hasLightDismiss: true,
@@ -270,20 +271,50 @@ export function TabMenu({
     // The popup's own role="menu" is the exposed semantics; a modal dialog
     // wrapper would announce an unnamed dialog around the menu.
     role: 'none',
+    // Return focus to the trigger when the menu closes (Escape, Tab, select,
+    // or light dismiss) so keyboard focus is never dropped to <body>.
+    onHide: useCallback(() => {
+      buttonRef.current?.focus();
+    }, []),
   });
 
-  const {listRef, handleKeyDown: handleListKeyDown} =
-    useListFocus<HTMLDivElement>({
-      onEscape: () => popover.hide(),
-    });
+  // The overflow menu is a composite widget: a single roving tab stop with
+  // arrow-key navigation between items, per the APG menu pattern. The hook owns
+  // item tabindex — items render tabIndex={-1} and exactly one is promoted to 0.
+  const {
+    listRef,
+    handleKeyDown: handleListKeyDown,
+    handleFocus,
+    focusFirst,
+  } = useListFocus<HTMLDivElement>({
+    hasRovingTabIndex: true,
+    onEscape: () => popover.hide(),
+  });
 
   const handleToggle = useCallback(() => {
     if (popover.isOpen) {
       popover.hide();
     } else {
       popover.show();
+      // Move focus into the menu on open so arrow navigation works and the
+      // roving tab stop lands on a real item (APG menu-button focus-on-open).
+      requestAnimationFrame(() => focusFirst());
     }
-  }, [popover]);
+  }, [popover, focusFirst]);
+
+  const handleMenuKeyDown = useCallback(
+    (e: React.KeyboardEvent) => {
+      // APG menu-button: Tab leaves the menu rather than walking its items.
+      // Close and let onHide return focus to the trigger, from which the
+      // browser's default Tab continues to the next element.
+      if (e.key === 'Tab') {
+        popover.hide();
+        return;
+      }
+      handleListKeyDown(e);
+    },
+    [handleListKeyDown, popover],
+  );
 
   const selectedOption = options.find(o => o.value === tabListCtx.value);
   const triggerLabel = selectedOption?.label ?? label;
@@ -299,7 +330,11 @@ export function TabMenu({
     [tabListCtx, popover],
   );
 
-  const setButtonRef = mergeRefs<HTMLButtonElement>(popover.triggerRef, ref);
+  const setButtonRef = mergeRefs<HTMLButtonElement>(
+    popover.triggerRef,
+    buttonRef,
+    ref,
+  );
 
   return (
     <>
@@ -357,7 +392,8 @@ export function TabMenu({
           id={menuId}
           role="menu"
           aria-label={label}
-          onKeyDown={handleListKeyDown}
+          onKeyDown={handleMenuKeyDown}
+          onFocus={handleFocus}
           {...mergeProps(
             themeProps('tab-menu-dropdown'),
             stylex.props(styles.dropdown),
@@ -371,7 +407,7 @@ export function TabMenu({
               <div
                 key={option.value}
                 role="menuitem"
-                tabIndex={0}
+                tabIndex={-1}
                 aria-current={isSelected ? 'true' : undefined}
                 onClick={() => handleSelect(option.value)}
                 onKeyDown={e => {