diff --git a/packages/block-editor/src/components/block-list/insertion-point.js b/packages/block-editor/src/components/block-list/insertion-point.js
index f2842aa5b11d50..d759d568efd3e9 100644
--- a/packages/block-editor/src/components/block-list/insertion-point.js
+++ b/packages/block-editor/src/components/block-list/insertion-point.js
@@ -200,6 +200,18 @@ function InsertionPointPopover( {
 		}
 	}
 
+	// Only show the inserter when there's a `nextElement` (a block after the
+	// insertion point). At the end of the block list the trailing appender
+	// should serve the purpose of inserting blocks.
+	const showInsertionPointInserter =
+		! isHidden && nextElement && ( isInserterShown || isInserterForced );
+
+	// Show the indicator if the insertion point inserter is visible, or if
+	// the `showInsertionPoint` state is `true`. The latter is generally true
+	// when hovering blocks for insertion in the block library.
+	const showInsertionPointIndicator =
+		showInsertionPointInserter || ( ! isHidden && showInsertionPoint );
+
 	/* eslint-disable jsx-a11y/no-static-element-interactions, jsx-a11y/click-events-have-key-events */
 	// While ideally it would be enough to capture the
 	// bubbling focus event from the Inserter, due to the
@@ -224,13 +236,10 @@ function InsertionPointPopover( {
 				className={ className }
 				style={ style }
 			>
-				{ ! isHidden &&
-					( showInsertionPoint ||
-						isInserterShown ||
-						isInserterForced ) && (
-						<div className="block-editor-block-list__insertion-point-indicator" />
-					) }
-				{ ! isHidden && ( isInserterShown || isInserterForced ) && (
+				{ showInsertionPointIndicator && (
+					<div className="block-editor-block-list__insertion-point-indicator" />
+				) }
+				{ showInsertionPointInserter && (
 					<InsertionPointInserter
 						rootClientId={ rootClientId }
 						clientId={ nextClientId }
diff --git a/packages/e2e-tests/specs/experiments/document-settings.test.js b/packages/e2e-tests/specs/experiments/document-settings.test.js
index eb59dc2a3f82c2..8d7092d18c6592 100644
--- a/packages/e2e-tests/specs/experiments/document-settings.test.js
+++ b/packages/e2e-tests/specs/experiments/document-settings.test.js
@@ -1,11 +1,7 @@
 /**
  * WordPress dependencies
  */
-import {
-	canvas,
-	trashAllPosts,
-	activateTheme,
-} from '@wordpress/e2e-test-utils';
+import { trashAllPosts, activateTheme } from '@wordpress/e2e-test-utils';
 
 /**
  * Internal dependencies
@@ -58,9 +54,15 @@ describe( 'Document Settings', () => {
 
 		describe( 'and a template part is clicked in the template', () => {
 			it( "should display the selected template part's name in the document header", async () => {
-				// Click on a template part in the template
-				const header = await canvas().$( '.site-header' );
-				await header.click();
+				// Select the header template part via list view.
+				await page.click( 'button[aria-label="List View"]' );
+				const headerTemplatePartListViewButton = await page.waitForXPath(
+					'//button[contains(@class, "block-editor-block-navigation-block-select-button")][contains(., "Header")]'
+				);
+				headerTemplatePartListViewButton.click();
+				await page.click(
+					'button[aria-label="Close list view sidebar"]'
+				);
 
 				// Evaluate the document settings secondary title
 				const actual = await getDocumentSettingsSecondaryTitle();
diff --git a/packages/e2e-tests/specs/experiments/multi-entity-saving.test.js b/packages/e2e-tests/specs/experiments/multi-entity-saving.test.js
index c0c035ccd0894d..65e94a80711d7c 100644
--- a/packages/e2e-tests/specs/experiments/multi-entity-saving.test.js
+++ b/packages/e2e-tests/specs/experiments/multi-entity-saving.test.js
@@ -7,7 +7,6 @@ import {
 	publishPost,
 	trashAllPosts,
 	activateTheme,
-	canvas,
 } from '@wordpress/e2e-test-utils';
 
 /**
@@ -189,9 +188,13 @@ describe( 'Multi-entity save flow', () => {
 			await navigationPanel.clickItemByText( 'Index' );
 			await navigationPanel.close();
 
-			// Click the first block so that the template part inserts in the right place.
-			const firstBlock = await canvas().$( '.wp-block' );
-			await firstBlock.click();
+			// Select the header template part via list view.
+			await page.click( 'button[aria-label="List View"]' );
+			const headerTemplatePartListViewButton = await page.waitForXPath(
+				'//button[contains(@class, "block-editor-block-navigation-block-select-button")][contains(., "Header")]'
+			);
+			headerTemplatePartListViewButton.click();
+			await page.click( 'button[aria-label="Close list view sidebar"]' );
 
 			// Insert something to dirty the editor.
 			await insertBlock( 'Paragraph' );