diff --git a/packages/block-editor/src/components/block-list/use-block-props/index.js b/packages/block-editor/src/components/block-list/use-block-props/index.js
index 91c27c025b4a6..627f848ebf841 100644
--- a/packages/block-editor/src/components/block-list/use-block-props/index.js
+++ b/packages/block-editor/src/components/block-list/use-block-props/index.js
@@ -26,7 +26,8 @@ import { useBlockClassNames } from './use-block-class-names';
 import { useBlockDefaultClassName } from './use-block-default-class-name';
 import { useBlockCustomClassName } from './use-block-custom-class-name';
 import { useBlockMovingModeClassNames } from './use-block-moving-mode-class-names';
-import { useEventHandlers } from './use-event-handlers';
+import { useFocusHandler } from './use-focus-handler';
+import { useEventHandlers } from './use-selected-block-event-handlers';
 import { useNavModeExit } from './use-nav-mode-exit';
 import { useBlockNodes } from './use-block-nodes';
 import { useScrollIntoView } from './use-scroll-into-view';
@@ -106,6 +107,7 @@ export function useBlockProps( props = {}, { __unstableIsHtml } = {} ) {
 		// Must happen after focus because we check for focus in the block.
 		useScrollIntoView( clientId ),
 		useBlockNodes( clientId ),
+		useFocusHandler( clientId ),
 		useEventHandlers( clientId ),
 		useNavModeExit( clientId ),
 		useIsHovered(),
diff --git a/packages/block-editor/src/components/block-list/use-block-props/use-focus-handler.js b/packages/block-editor/src/components/block-list/use-block-props/use-focus-handler.js
new file mode 100644
index 0000000000000..4946cc40a26c9
--- /dev/null
+++ b/packages/block-editor/src/components/block-list/use-block-props/use-focus-handler.js
@@ -0,0 +1,56 @@
+/**
+ * WordPress dependencies
+ */
+import { useSelect, useDispatch } from '@wordpress/data';
+import { useRefEffect } from '@wordpress/compose';
+
+/**
+ * Internal dependencies
+ */
+import { isInsideRootBlock } from '../../../utils/dom';
+import { store as blockEditorStore } from '../../../store';
+
+/**
+ * Selects the block if it receives focus.
+ *
+ * @param {string} clientId Block client ID.
+ */
+export function useFocusHandler( clientId ) {
+	const { isBlockSelected } = useSelect( blockEditorStore );
+	const { selectBlock } = useDispatch( blockEditorStore );
+
+	return useRefEffect(
+		( node ) => {
+			/**
+			 * Marks the block as selected when focused and not already
+			 * selected. This specifically handles the case where block does not
+			 * set focus on its own (via `setFocus`), typically if there is no
+			 * focusable input in the block.
+			 *
+			 * @param {FocusEvent} event Focus event.
+			 */
+			function onFocus( event ) {
+				// Check synchronously because a non-selected block might be
+				// getting data through `useSelect` asynchronously.
+				if ( isBlockSelected( clientId ) ) {
+					return;
+				}
+
+				// If an inner block is focussed, that block is resposible for
+				// setting the selected block.
+				if ( ! isInsideRootBlock( node, event.target ) ) {
+					return;
+				}
+
+				selectBlock( clientId );
+			}
+
+			node.addEventListener( 'focusin', onFocus );
+
+			return () => {
+				node.removeEventListener( 'focusin', onFocus );
+			};
+		},
+		[ isBlockSelected, selectBlock ]
+	);
+}
diff --git a/packages/block-editor/src/components/block-list/use-block-props/use-event-handlers.js b/packages/block-editor/src/components/block-list/use-block-props/use-selected-block-event-handlers.js
similarity index 66%
rename from packages/block-editor/src/components/block-list/use-block-props/use-event-handlers.js
rename to packages/block-editor/src/components/block-list/use-block-props/use-selected-block-event-handlers.js
index 844a6862fd8eb..d5ee93fe3f988 100644
--- a/packages/block-editor/src/components/block-list/use-block-props/use-event-handlers.js
+++ b/packages/block-editor/src/components/block-list/use-block-props/use-selected-block-event-handlers.js
@@ -10,13 +10,11 @@ import { useRefEffect } from '@wordpress/compose';
 /**
  * Internal dependencies
  */
-import { isInsideRootBlock } from '../../../utils/dom';
 import { SelectionStart } from '../../writing-flow';
 import { store as blockEditorStore } from '../../../store';
 
 /**
  * Adds block behaviour:
- *   - Selects the block if it receives focus.
  *   - Removes the block on BACKSPACE.
  *   - Inserts a default block on ENTER.
  *   - Initiates selection start for multi-selection.
@@ -26,52 +24,19 @@ import { store as blockEditorStore } from '../../../store';
  */
 export function useEventHandlers( clientId ) {
 	const onSelectionStart = useContext( SelectionStart );
-	const { isSelected, rootClientId, index } = useSelect(
-		( select ) => {
-			const {
-				isBlockSelected,
-				getBlockRootClientId,
-				getBlockIndex,
-			} = select( blockEditorStore );
-
-			return {
-				isSelected: isBlockSelected( clientId ),
-				rootClientId: getBlockRootClientId( clientId ),
-				index: getBlockIndex( clientId ),
-			};
-		},
+	const isSelected = useSelect(
+		( select ) => select( blockEditorStore ).isBlockSelected( clientId ),
 		[ clientId ]
 	);
-	const { insertDefaultBlock, removeBlock, selectBlock } = useDispatch(
+	const { getBlockRootClientId, getBlockIndex } = useSelect(
 		blockEditorStore
 	);
+	const { insertDefaultBlock, removeBlock } = useDispatch( blockEditorStore );
 
 	return useRefEffect(
 		( node ) => {
 			if ( ! isSelected ) {
-				/**
-				 * Marks the block as selected when focused and not already
-				 * selected. This specifically handles the case where block does not
-				 * set focus on its own (via `setFocus`), typically if there is no
-				 * focusable input in the block.
-				 *
-				 * @param {FocusEvent} event Focus event.
-				 */
-				function onFocus( event ) {
-					// If an inner block is focussed, that block is resposible for
-					// setting the selected block.
-					if ( ! isInsideRootBlock( node, event.target ) ) {
-						return;
-					}
-
-					selectBlock( clientId );
-				}
-
-				node.addEventListener( 'focusin', onFocus );
-
-				return () => {
-					node.removeEventListener( 'focusin', onFocus );
-				};
+				return;
 			}
 
 			/**
@@ -101,7 +66,11 @@ export function useEventHandlers( clientId ) {
 				event.preventDefault();
 
 				if ( keyCode === ENTER ) {
-					insertDefaultBlock( {}, rootClientId, index + 1 );
+					insertDefaultBlock(
+						{},
+						getBlockRootClientId( clientId ),
+						getBlockIndex( clientId ) + 1
+					);
 				} else {
 					removeBlock( clientId );
 				}
@@ -136,13 +105,13 @@ export function useEventHandlers( clientId ) {
 			};
 		},
 		[
+			clientId,
 			isSelected,
-			rootClientId,
-			index,
+			getBlockRootClientId,
+			getBlockIndex,
 			onSelectionStart,
 			insertDefaultBlock,
 			removeBlock,
-			selectBlock,
 		]
 	);
 }
diff --git a/packages/block-editor/src/components/block-navigation/dropdown.js b/packages/block-editor/src/components/block-navigation/dropdown.js
index b72d879d6762e..6ffe00fc93f8d 100644
--- a/packages/block-editor/src/components/block-navigation/dropdown.js
+++ b/packages/block-editor/src/components/block-navigation/dropdown.js
@@ -80,9 +80,8 @@ function BlockNavigationDropdown(
 					isEnabled={ isEnabled }
 				/>
 			) }
-			renderContent={ ( { onClose } ) => (
+			renderContent={ () => (
 				<BlockNavigation
-					onSelect={ onClose }
 					__experimentalFeatures={ __experimentalFeatures }
 				/>
 			) }
diff --git a/packages/e2e-tests/specs/editor/blocks/list.test.js b/packages/e2e-tests/specs/editor/blocks/list.test.js
index 57d9fc40e7a3f..ddc115e2195c4 100644
--- a/packages/e2e-tests/specs/editor/blocks/list.test.js
+++ b/packages/e2e-tests/specs/editor/blocks/list.test.js
@@ -113,6 +113,7 @@ describe( 'List', () => {
 		await clickBlockAppender();
 		await page.keyboard.press( 'Enter' );
 		await page.keyboard.type( '* ' );
+		await page.evaluate( () => new Promise( window.requestIdleCallback ) );
 		await page.keyboard.press( 'ArrowUp' );
 		await page.keyboard.press( 'ArrowDown' );
 		await page.keyboard.press( 'Backspace' );