diff --git a/packages/block-editor/src/components/block-list-appender/index.js b/packages/block-editor/src/components/block-list-appender/index.js
index fae056e50dcb50..e2a4dbb0ebd6bc 100644
--- a/packages/block-editor/src/components/block-list-appender/index.js
+++ b/packages/block-editor/src/components/block-list-appender/index.js
@@ -7,7 +7,6 @@ import classnames from 'classnames';
 /**
  * WordPress dependencies
  */
-import { createContext, useContext } from '@wordpress/element';
 import { withSelect } from '@wordpress/data';
 import { getDefaultBlockName } from '@wordpress/blocks';
 
@@ -17,9 +16,6 @@ import { getDefaultBlockName } from '@wordpress/blocks';
 import DefaultBlockAppender from '../default-block-appender';
 import ButtonBlockAppender from '../button-block-appender';
 
-// A Context to store the map of the appender map.
-export const AppenderNodesContext = createContext();
-
 function stopPropagation( event ) {
 	event.stopPropagation();
 }
@@ -34,8 +30,6 @@ function BlockListAppender( {
 	selectedBlockClientId,
 	tagName: TagName = 'div',
 } ) {
-	const appenderNodesMap = useContext( AppenderNodesContext );
-
 	if ( isLocked || CustomAppender === false ) {
 		return null;
 	}
@@ -95,20 +89,7 @@ function BlockListAppender( {
 			// Prevent the block from being selected when the appender is
 			// clicked.
 			onFocus={ stopPropagation }
-			className={ classnames(
-				'block-list-appender',
-				'wp-block',
-				className
-			) }
-			ref={ ( ref ) => {
-				if ( ref ) {
-					// Set the reference of the "Appender" with `rootClientId` as key.
-					appenderNodesMap.set( rootClientId || '', ref );
-				} else {
-					// If it un-mounts, cleanup the map.
-					appenderNodesMap.delete( rootClientId || '' );
-				}
-			} }
+			className={ classnames( 'block-list-appender', className ) }
 		>
 			{ appender }
 		</TagName>
diff --git a/packages/block-editor/src/components/block-list/index.js b/packages/block-editor/src/components/block-list/index.js
index c74ed80bb074b7..22ede3bc48e677 100644
--- a/packages/block-editor/src/components/block-list/index.js
+++ b/packages/block-editor/src/components/block-list/index.js
@@ -13,17 +13,10 @@ import { useRef, forwardRef } from '@wordpress/element';
  * Internal dependencies
  */
 import BlockListBlock from './block';
-import BlockListAppender, {
-	AppenderNodesContext,
-} from '../block-list-appender';
+import BlockListAppender from '../block-list-appender';
 import RootContainer from './root-container';
 import useBlockDropZone from '../use-block-drop-zone';
 
-/**
- * A map to store the reference of each "Appenders" rendered with `rootClientId` as key.
- */
-const appenderNodesMap = new Map();
-
 /**
  * If the block count exceeds the threshold, we disable the reordering animation
  * to avoid laginess.
@@ -89,60 +82,57 @@ function BlockList(
 		dropTargetIndex === blockClientIds.length && isDraggingBlocks;
 
 	return (
-		<AppenderNodesContext.Provider value={ appenderNodesMap }>
-			<Container
-				{ ...__experimentalPassedProps }
-				ref={ element }
-				className={ classnames(
-					'block-editor-block-list__layout',
-					className,
-					__experimentalPassedProps.className
-				) }
-			>
-				{ blockClientIds.map( ( clientId, index ) => {
-					const isBlockInSelection = hasMultiSelection
-						? multiSelectedBlockClientIds.includes( clientId )
-						: selectedBlockClientId === clientId;
+		<Container
+			{ ...__experimentalPassedProps }
+			ref={ element }
+			className={ classnames(
+				'block-editor-block-list__layout',
+				className,
+				__experimentalPassedProps.className
+			) }
+		>
+			{ blockClientIds.map( ( clientId, index ) => {
+				const isBlockInSelection = hasMultiSelection
+					? multiSelectedBlockClientIds.includes( clientId )
+					: selectedBlockClientId === clientId;
 
-					const isDropTarget =
-						dropTargetIndex === index && isDraggingBlocks;
+				const isDropTarget =
+					dropTargetIndex === index && isDraggingBlocks;
 
-					return (
-						<AsyncModeProvider
-							key={ clientId }
-							value={ ! isBlockInSelection }
-						>
-							<BlockListBlock
-								rootClientId={ rootClientId }
-								clientId={ clientId }
-								// This prop is explicitely computed and passed down
-								// to avoid being impacted by the async mode
-								// otherwise there might be a small delay to trigger the animation.
-								index={ index }
-								enableAnimation={ enableAnimation }
-								className={ classnames( {
-									'is-drop-target': isDropTarget,
-									'is-dropping-horizontally':
-										isDropTarget &&
-										orientation === 'horizontal',
-								} ) }
-							/>
-						</AsyncModeProvider>
-					);
+				return (
+					<AsyncModeProvider
+						key={ clientId }
+						value={ ! isBlockInSelection }
+					>
+						<BlockListBlock
+							rootClientId={ rootClientId }
+							clientId={ clientId }
+							// This prop is explicitely computed and passed down
+							// to avoid being impacted by the async mode
+							// otherwise there might be a small delay to trigger the animation.
+							index={ index }
+							enableAnimation={ enableAnimation }
+							className={ classnames( {
+								'is-drop-target': isDropTarget,
+								'is-dropping-horizontally':
+									isDropTarget &&
+									orientation === 'horizontal',
+							} ) }
+						/>
+					</AsyncModeProvider>
+				);
+			} ) }
+			<BlockListAppender
+				tagName={ __experimentalAppenderTagName }
+				rootClientId={ rootClientId }
+				renderAppender={ renderAppender }
+				className={ classnames( {
+					'is-drop-target': isAppenderDropTarget,
+					'is-dropping-horizontally':
+						isAppenderDropTarget && orientation === 'horizontal',
 				} ) }
-				<BlockListAppender
-					tagName={ __experimentalAppenderTagName }
-					rootClientId={ rootClientId }
-					renderAppender={ renderAppender }
-					className={ classnames( {
-						'is-drop-target': isAppenderDropTarget,
-						'is-dropping-horizontally':
-							isAppenderDropTarget &&
-							orientation === 'horizontal',
-					} ) }
-				/>
-			</Container>
-		</AppenderNodesContext.Provider>
+			/>
+		</Container>
 	);
 }
 
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 ebfc46a22a3d06..8562b088bb9ee4 100644
--- a/packages/block-editor/src/components/block-list/insertion-point.js
+++ b/packages/block-editor/src/components/block-list/insertion-point.js
@@ -7,7 +7,7 @@ import classnames from 'classnames';
  * WordPress dependencies
  */
 import { useSelect } from '@wordpress/data';
-import { useState, useRef, useMemo, useContext } from '@wordpress/element';
+import { useState, useRef } from '@wordpress/element';
 import { Popover } from '@wordpress/components';
 import { placeCaretAtVerticalEdge } from '@wordpress/dom';
 
@@ -17,7 +17,6 @@ import { placeCaretAtVerticalEdge } from '@wordpress/dom';
 import Inserter from '../inserter';
 import { getClosestTabbable } from '../writing-flow';
 import { getBlockDOMNode } from '../../utils/dom';
-import { AppenderNodesContext } from '../block-list-appender';
 
 function InsertionPointInserter( {
 	clientId,
@@ -99,24 +98,13 @@ function InsertionPointInserter( {
 
 function InsertionPointPopover( {
 	clientId,
-	rootClientId,
 	isInserterShown,
 	isInserterForced,
 	setIsInserterForced,
 	containerRef,
 	showInsertionPoint,
 } ) {
-	const appenderNodesMap = useContext( AppenderNodesContext );
-	const element = useMemo( () => {
-		if ( clientId ) {
-			return getBlockDOMNode( clientId );
-		}
-
-		// Can't find the element, might be at the end of the block list, or inside an empty block list.
-		// We instead try to find the "Appender" and place the indicator above it.
-		// `rootClientId` could be null or undefined when there's no parent block, we normalize it to an empty string.
-		return appenderNodesMap.get( rootClientId || '' );
-	}, [ clientId, rootClientId, appenderNodesMap ] );
+	const element = getBlockDOMNode( clientId );
 
 	return (
 		<Popover
@@ -151,29 +139,26 @@ export default function InsertionPoint( { children, containerRef } ) {
 	const [ isInserterShown, setIsInserterShown ] = useState( false );
 	const [ isInserterForced, setIsInserterForced ] = useState( false );
 	const [ inserterClientId, setInserterClientId ] = useState( null );
-	const {
-		isMultiSelecting,
-		isInserterVisible,
-		selectedClientId,
-		selectedRootClientId,
-	} = useSelect( ( select ) => {
-		const {
-			isMultiSelecting: _isMultiSelecting,
-			isBlockInsertionPointVisible,
-			getBlockInsertionPoint,
-			getBlockOrder,
-		} = select( 'core/block-editor' );
-
-		const insertionPoint = getBlockInsertionPoint();
-		const order = getBlockOrder( insertionPoint.rootClientId );
-
-		return {
-			isMultiSelecting: _isMultiSelecting(),
-			isInserterVisible: isBlockInsertionPointVisible(),
-			selectedClientId: order[ insertionPoint.index ],
-			selectedRootClientId: insertionPoint.rootClientId,
-		};
-	}, [] );
+	const { isMultiSelecting, isInserterVisible, selectedClientId } = useSelect(
+		( select ) => {
+			const {
+				isMultiSelecting: _isMultiSelecting,
+				isBlockInsertionPointVisible,
+				getBlockInsertionPoint,
+				getBlockOrder,
+			} = select( 'core/block-editor' );
+
+			const insertionPoint = getBlockInsertionPoint();
+			const order = getBlockOrder( insertionPoint.rootClientId );
+
+			return {
+				isMultiSelecting: _isMultiSelecting(),
+				isInserterVisible: isBlockInsertionPointVisible(),
+				selectedClientId: order[ insertionPoint.index ],
+			};
+		},
+		[]
+	);
 
 	function onMouseMove( event ) {
 		if (
@@ -230,7 +215,6 @@ export default function InsertionPoint( { children, containerRef } ) {
 					clientId={
 						isInserterVisible ? selectedClientId : inserterClientId
 					}
-					rootClientId={ selectedRootClientId }
 					isInserterShown={ isInserterShown }
 					isInserterForced={ isInserterForced }
 					setIsInserterForced={ setIsInserterForced }
diff --git a/packages/block-editor/src/components/block-list/style.scss b/packages/block-editor/src/components/block-list/style.scss
index 77b2a30a9dab8f..ad60dd086b12ca 100644
--- a/packages/block-editor/src/components/block-list/style.scss
+++ b/packages/block-editor/src/components/block-list/style.scss
@@ -365,10 +365,6 @@
 	position: relative;
 	z-index: z-index(".block-editor-block-list__insertion-point");
 	margin-top: -$block-padding * 2;
-
-	&.is-insert-after {
-		margin-top: $block-padding;
-	}
 }
 
 .block-editor-block-list__insertion-point-indicator {
diff --git a/packages/e2e-tests/specs/editor/various/adding-blocks.test.js b/packages/e2e-tests/specs/editor/various/adding-blocks.test.js
index be849af8d01250..d6d1496da80a76 100644
--- a/packages/e2e-tests/specs/editor/various/adding-blocks.test.js
+++ b/packages/e2e-tests/specs/editor/various/adding-blocks.test.js
@@ -8,7 +8,6 @@ import {
 	pressKeyTimes,
 	setBrowserViewport,
 	closeGlobalBlockInserter,
-	searchForBlock,
 } from '@wordpress/e2e-test-utils';
 
 /** @typedef {import('puppeteer').ElementHandle} ElementHandle */
@@ -263,36 +262,4 @@ describe( 'adding blocks', () => {
 		await coverBlock.click();
 		expect( await getEditedPostContent() ).toMatchSnapshot();
 	} );
-
-	// Check for regression of https://github.com/WordPress/gutenberg/issues/25785
-	it( 'inserts a block should show a blue line indicator', async () => {
-		// First insert a random Paragraph.
-		await insertBlock( 'Paragraph' );
-		await page.keyboard.type( 'First paragraph' );
-
-		// Open the global inserter and search for the Heading block.
-		await searchForBlock( 'Heading' );
-
-		const headingButton = (
-			await page.$x( `//button//span[contains(text(), 'Heading')]` )
-		 )[ 0 ];
-
-		// Hover over the block should show the blue line indicator.
-		await headingButton.hover();
-
-		// Should show the blue line indicator somewhere.
-		const indicator = await page.$(
-			'.block-editor-block-list__insertion-point-indicator'
-		);
-		const indicatorRect = await indicator.boundingBox();
-
-		const paragraphBlock = await page.$(
-			'p[aria-label="Paragraph block"]'
-		);
-		const paragraphRect = await paragraphBlock.boundingBox();
-
-		// The blue line indicator should be below the last block.
-		expect( indicatorRect.x ).toBe( paragraphRect.x );
-		expect( indicatorRect.y > paragraphRect.y ).toBe( true );
-	} );
 } );
diff --git a/packages/edit-widgets/src/blocks/widget-area/edit/inner-blocks.js b/packages/edit-widgets/src/blocks/widget-area/edit/inner-blocks.js
index 7b27a404a2f6c8..cf23812646eac8 100644
--- a/packages/edit-widgets/src/blocks/widget-area/edit/inner-blocks.js
+++ b/packages/edit-widgets/src/blocks/widget-area/edit/inner-blocks.js
@@ -15,7 +15,6 @@ export default function WidgetAreaInnerBlocks() {
 			onInput={ onInput }
 			onChange={ onChange }
 			templateLock={ false }
-			renderAppender={ InnerBlocks.DefaultBlockAppender }
 		/>
 	);
 }