diff --git a/packages/block-editor/src/components/inner-blocks/use-inner-block-template-sync.js b/packages/block-editor/src/components/inner-blocks/use-inner-block-template-sync.js
index 1b81069c44f3dc..c9ccfe7faaf0e4 100644
--- a/packages/block-editor/src/components/inner-blocks/use-inner-block-template-sync.js
+++ b/packages/block-editor/src/components/inner-blocks/use-inner-block-template-sync.js
@@ -42,7 +42,8 @@ export default function useInnerBlockTemplateSync(
 ) {
 	const { getSelectedBlocksInitialCaretPosition, isBlockSelected } =
 		useSelect( blockEditorStore );
-	const { replaceInnerBlocks } = useDispatch( blockEditorStore );
+	const { replaceInnerBlocks, __unstableMarkNextChangeAsNotPersistent } =
+		useDispatch( blockEditorStore );
 	const innerBlocks = useSelect(
 		( select ) => select( blockEditorStore ).getBlocks( clientId ),
 		[ clientId ]
@@ -81,6 +82,7 @@ export default function useInnerBlockTemplateSync(
 			);
 
 			if ( ! isEqual( nextBlocks, currentInnerBlocks ) ) {
+				__unstableMarkNextChangeAsNotPersistent();
 				replaceInnerBlocks(
 					clientId,
 					nextBlocks,
diff --git a/packages/e2e-tests/plugins/inner-blocks-templates/index.js b/packages/e2e-tests/plugins/inner-blocks-templates/index.js
index 3d8630103f16a1..959f4a3eeb5a0b 100644
--- a/packages/e2e-tests/plugins/inner-blocks-templates/index.js
+++ b/packages/e2e-tests/plugins/inner-blocks-templates/index.js
@@ -3,6 +3,8 @@
 	const createBlock = wp.blocks.createBlock;
 	const el = wp.element.createElement;
 	const InnerBlocks = wp.blockEditor.InnerBlocks;
+	const useState = window.wp.element.useState;
+
 	const TEMPLATE = [
 		[
 			'core/paragraph',
@@ -171,4 +173,31 @@
 
 		save,
 	} );
+
+
+	function InnerBlocksAsyncTemplateEdit() {
+		const [ template, setTemplate ] = useState( [] );
+
+		setInterval( () => {
+			setTemplate( TEMPLATE_TWO_PARAGRAPHS );
+		}, 1000 );
+
+		return el( InnerBlocks, {
+			template,
+		} );
+	}
+
+	registerBlockType(
+		'test/test-inner-blocks-async-template',
+		{
+			title: 'Test Inner Blocks Async Template',
+			icon: 'cart',
+			category: 'text',
+
+			edit: InnerBlocksAsyncTemplateEdit,
+
+			// Purposely do not save inner blocks so that it's possible to test template resolution.
+			save() {},
+		}
+	);
 } )();
diff --git a/test/e2e/specs/editor/plugins/__snapshots__/templates-Using-a-CPT-with-a-predefined-templa-7538a--custom-post-types-with-a-predefined-template-1-chromium.txt b/test/e2e/specs/editor/plugins/__snapshots__/Post-type-templates-Using-a-CPT-with-a-predefi-fffe1--custom-post-types-with-a-predefined-template-1-chromium.txt
similarity index 100%
rename from test/e2e/specs/editor/plugins/__snapshots__/templates-Using-a-CPT-with-a-predefined-templa-7538a--custom-post-types-with-a-predefined-template-1-chromium.txt
rename to test/e2e/specs/editor/plugins/__snapshots__/Post-type-templates-Using-a-CPT-with-a-predefi-fffe1--custom-post-types-with-a-predefined-template-1-chromium.txt
diff --git a/test/e2e/specs/editor/plugins/templates.spec.js b/test/e2e/specs/editor/plugins/post-type-templates.spec.js
similarity index 98%
rename from test/e2e/specs/editor/plugins/templates.spec.js
rename to test/e2e/specs/editor/plugins/post-type-templates.spec.js
index bab5cdd739baf6..3c5a664259f2d2 100644
--- a/test/e2e/specs/editor/plugins/templates.spec.js
+++ b/test/e2e/specs/editor/plugins/post-type-templates.spec.js
@@ -3,7 +3,7 @@
  */
 const { test, expect } = require( '@wordpress/e2e-test-utils-playwright' );
 
-test.describe( 'templates', () => {
+test.describe( 'Post type templates', () => {
 	test.describe( 'Using a CPT with a predefined template', () => {
 		test.beforeAll( async ( { requestUtils } ) => {
 			await requestUtils.activatePlugin(
diff --git a/test/e2e/specs/editor/various/inner-blocks-templates.spec.js b/test/e2e/specs/editor/various/inner-blocks-templates.spec.js
new file mode 100644
index 00000000000000..87ad2604281983
--- /dev/null
+++ b/test/e2e/specs/editor/various/inner-blocks-templates.spec.js
@@ -0,0 +1,56 @@
+/**
+ * WordPress dependencies
+ */
+const { test, expect } = require( '@wordpress/e2e-test-utils-playwright' );
+
+test.describe( 'Inner blocks templates', () => {
+	test.beforeAll( async ( { requestUtils } ) => {
+		await requestUtils.activatePlugin(
+			'gutenberg-test-inner-blocks-templates'
+		);
+	} );
+
+	test.beforeEach( async ( { admin } ) => {
+		await admin.createNewPost();
+	} );
+
+	test.afterAll( async ( { requestUtils } ) => {
+		await requestUtils.deactivatePlugin(
+			'gutenberg-test-inner-blocks-templates'
+		);
+	} );
+
+	test( 'applying block templates asynchronously does not create a persistent change in the editor', async ( {
+		editor,
+		page,
+	} ) => {
+		await editor.insertBlock( {
+			name: 'test/test-inner-blocks-async-template',
+		} );
+
+		const blockWithTemplateContent = page.locator(
+			'role=document[name="Block: Test Inner Blocks Async Template"i] >> text=OneTwo'
+		);
+
+		// The block template content appears asynchronously, so wait for it.
+		await expect( blockWithTemplateContent ).toBeVisible();
+
+		// Publish the post, then reload.
+		await editor.publishPost();
+		await page.reload();
+
+		// Wait for the block that was inserted to appear with its templated content.
+		await expect( blockWithTemplateContent ).toBeVisible();
+
+		// The template resolution shouldn't cause the post to be dirty.
+		const editorTopBar = page.locator(
+			'role=region[name="Editor top bar"i]'
+		);
+		const undoButton = editorTopBar.locator( 'role=button[name="Undo"i]' );
+		const updateButton = editorTopBar.locator(
+			'role=button[name="Update"i]'
+		);
+		await expect( undoButton ).toHaveAttribute( 'aria-disabled', 'true' );
+		await expect( updateButton ).toHaveAttribute( 'aria-disabled', 'true' );
+	} );
+} );