diff --git a/packages/components/CHANGELOG.md b/packages/components/CHANGELOG.md
index c4153503fd798..ae1951685f68e 100644
--- a/packages/components/CHANGELOG.md
+++ b/packages/components/CHANGELOG.md
@@ -16,6 +16,10 @@
 -   `ToggleGroupControl`: react correctly to external controlled updates ([#56678](https://github.com/WordPress/gutenberg/pull/56678)).
 -   `ToolsPanel`: fix a performance issue ([#56770](https://github.com/WordPress/gutenberg/pull/56770)).
 
+### Experimental
+
+-   `Tabs`: improve focus handling in controlled mode ([#56658](https://github.com/WordPress/gutenberg/pull/56658)).
+
 ## 25.13.0 (2023-11-29)
 
 ### Enhancements
diff --git a/packages/components/src/tabs/index.tsx b/packages/components/src/tabs/index.tsx
index 12dd0b4fcc83f..7f738cb9f08a9 100644
--- a/packages/components/src/tabs/index.tsx
+++ b/packages/components/src/tabs/index.tsx
@@ -45,7 +45,7 @@ function Tabs( {
 	const isControlled = selectedTabId !== undefined;
 
 	const { items, selectedId } = store.useState();
-	const { setSelectedId } = store;
+	const { setSelectedId, move } = store;
 
 	// Keep track of whether tabs have been populated. This is used to prevent
 	// certain effects from firing too early while tab data and relevant
@@ -154,6 +154,27 @@ function Tabs( {
 		setSelectedId,
 	] );
 
+	// In controlled mode, make sure browser focus follows the selected tab if
+	// the selection is changed while a tab is already being focused.
+	useLayoutEffect( () => {
+		if ( ! isControlled || ! selectOnMove ) {
+			return;
+		}
+		const currentItem = items.find( ( item ) => item.id === selectedId );
+		const activeElement = currentItem?.element?.ownerDocument.activeElement;
+		const tabsHasFocus = items.some( ( item ) => {
+			return activeElement && activeElement === item.element;
+		} );
+
+		if (
+			activeElement &&
+			tabsHasFocus &&
+			selectedId !== activeElement.id
+		) {
+			move( selectedId );
+		}
+	}, [ isControlled, items, move, selectOnMove, selectedId ] );
+
 	const contextValue = useMemo(
 		() => ( {
 			store,
diff --git a/packages/components/src/tabs/test/index.tsx b/packages/components/src/tabs/test/index.tsx
index f923dc455fd7b..0f7b9271b450a 100644
--- a/packages/components/src/tabs/test/index.tsx
+++ b/packages/components/src/tabs/test/index.tsx
@@ -7,7 +7,7 @@ import { press, click } from '@ariakit/test';
 /**
  * WordPress dependencies
  */
-import { useState } from '@wordpress/element';
+import { useEffect, useState } from '@wordpress/element';
 
 /**
  * Internal dependencies
@@ -102,6 +102,10 @@ const ControlledTabs = ( {
 		string | undefined | null
 	>( props.selectedTabId );
 
+	useEffect( () => {
+		setSelectedTabId( props.selectedTabId );
+	}, [ props.selectedTabId ] );
+
 	return (
 		<Tabs
 			{ ...props }
@@ -1168,5 +1172,110 @@ describe( 'Tabs', () => {
 				).not.toBeInTheDocument();
 			} );
 		} );
+
+		describe( 'When `selectOnMove` is `true`', () => {
+			it( 'should automatically select a newly focused tab', async () => {
+				render( <ControlledTabs tabs={ TABS } selectedTabId="beta" /> );
+
+				await press.Tab();
+
+				// Tab key should focus the currently selected tab, which is Beta.
+				expect( await getSelectedTab() ).toHaveTextContent( 'Beta' );
+				expect( await getSelectedTab() ).toHaveFocus();
+
+				// Arrow keys should select and move focus to the next tab.
+				await press.ArrowRight();
+				expect( await getSelectedTab() ).toHaveTextContent( 'Gamma' );
+				expect( await getSelectedTab() ).toHaveFocus();
+			} );
+			it( 'should automatically update focus when the selected tab is changed by the controlling component', async () => {
+				const { rerender } = render(
+					<ControlledTabs tabs={ TABS } selectedTabId="beta" />
+				);
+
+				// Tab key should focus the currently selected tab, which is Beta.
+				await press.Tab();
+				expect( await getSelectedTab() ).toHaveTextContent( 'Beta' );
+				expect( await getSelectedTab() ).toHaveFocus();
+
+				rerender(
+					<ControlledTabs tabs={ TABS } selectedTabId="gamma" />
+				);
+
+				// When the selected tab is changed, it should automatically receive focus.
+				expect( await getSelectedTab() ).toHaveTextContent( 'Gamma' );
+				expect( await getSelectedTab() ).toHaveFocus();
+			} );
+		} );
+		describe( 'When `selectOnMove` is `false`', () => {
+			it( 'should apply focus without automatically changing the selected tab', async () => {
+				render(
+					<ControlledTabs
+						tabs={ TABS }
+						selectedTabId="beta"
+						selectOnMove={ false }
+					/>
+				);
+
+				expect( await getSelectedTab() ).toHaveTextContent( 'Beta' );
+
+				// Tab key should focus the currently selected tab, which is Beta.
+				await press.Tab();
+				expect(
+					await screen.findByRole( 'tab', { name: 'Beta' } )
+				).toHaveFocus();
+
+				// Arrow key should move focus but not automatically change the selected tab.
+				await press.ArrowRight();
+				expect(
+					screen.getByRole( 'tab', { name: 'Gamma' } )
+				).toHaveFocus();
+				expect( await getSelectedTab() ).toHaveTextContent( 'Beta' );
+
+				// Pressing the spacebar should select the focused tab.
+				await press.Space();
+				expect( await getSelectedTab() ).toHaveTextContent( 'Gamma' );
+
+				// Arrow key should move focus but not automatically change the selected tab.
+				await press.ArrowRight();
+				expect(
+					screen.getByRole( 'tab', { name: 'Alpha' } )
+				).toHaveFocus();
+				expect( await getSelectedTab() ).toHaveTextContent( 'Gamma' );
+
+				// Pressing the enter/return should select the focused tab.
+				await press.Enter();
+				expect( await getSelectedTab() ).toHaveTextContent( 'Alpha' );
+			} );
+			it( 'should not automatically update focus when the selected tab is changed by the controlling component', async () => {
+				const { rerender } = render(
+					<ControlledTabs
+						tabs={ TABS }
+						selectedTabId="beta"
+						selectOnMove={ false }
+					/>
+				);
+
+				expect( await getSelectedTab() ).toHaveTextContent( 'Beta' );
+
+				// Tab key should focus the currently selected tab, which is Beta.
+				await press.Tab();
+				expect( await getSelectedTab() ).toHaveFocus();
+
+				rerender(
+					<ControlledTabs
+						tabs={ TABS }
+						selectedTabId="gamma"
+						selectOnMove={ false }
+					/>
+				);
+
+				// When the selected tab is changed, it should not automatically receive focus.
+				expect( await getSelectedTab() ).toHaveTextContent( 'Gamma' );
+				expect(
+					screen.getByRole( 'tab', { name: 'Beta' } )
+				).toHaveFocus();
+			} );
+		} );
 	} );
 } );