diff --git a/packages/block-editor/src/components/block-list/block-popover.js b/packages/block-editor/src/components/block-list/block-popover.js
index d197e663964791..2919019d849a9e 100644
--- a/packages/block-editor/src/components/block-list/block-popover.js
+++ b/packages/block-editor/src/components/block-list/block-popover.js
@@ -20,7 +20,7 @@ import { useViewportMatch } from '@wordpress/compose';
 import BlockBreadcrumb from './breadcrumb';
 import BlockContextualToolbar from './block-contextual-toolbar';
 import Inserter from '../inserter';
-import { SelectedBlockNode } from './root-container';
+import { BlockNodes } from './root-container';
 
 function selector( select ) {
 	const {
@@ -30,6 +30,7 @@ function selector( select ) {
 		isTyping,
 		isCaretWithinFormattedText,
 		getSettings,
+		getLastMultiSelectedBlockClientId,
 	} = select( 'core/block-editor' );
 	return {
 		isNavigationMode: isNavigationMode(),
@@ -38,6 +39,7 @@ function selector( select ) {
 		isCaretWithinFormattedText: isCaretWithinFormattedText(),
 		hasMultiSelection: hasMultiSelection(),
 		hasFixedToolbar: getSettings().hasFixedToolbar,
+		lastClientId: getLastMultiSelectedBlockClientId(),
 	};
 }
 
@@ -58,11 +60,12 @@ function BlockPopover( {
 		isCaretWithinFormattedText,
 		hasMultiSelection,
 		hasFixedToolbar,
+		lastClientId,
 	} = useSelect( selector, [] );
 	const isLargeViewport = useViewportMatch( 'medium' );
 	const [ isToolbarForced, setIsToolbarForced ] = useState( false );
 	const [ isInserterShown, setIsInserterShown ] = useState( false );
-	let [ node ] = useContext( SelectedBlockNode );
+	const [ blockNodes ] = useContext( BlockNodes );
 
 	const showEmptyBlockSideInserter = ! isNavigationMode && isEmptyDefaultBlock && isValid;
 	const shouldShowBreadcrumb = isNavigationMode;
@@ -94,6 +97,8 @@ function BlockPopover( {
 		return null;
 	}
 
+	let node = blockNodes[ clientId ];
+
 	if ( capturingClientId ) {
 		node = document.getElementById( 'block-' + capturingClientId );
 	}
@@ -107,6 +112,15 @@ function BlockPopover( {
 		node = node.querySelector( '.is-block-content' ) || node;
 	}
 
+	let anchorRef = node;
+
+	if ( hasMultiSelection ) {
+		anchorRef = {
+			top: blockNodes[ clientId ],
+			bottom: blockNodes[ lastClientId ],
+		};
+	}
+
 	function onFocus() {
 		setIsInserterShown( true );
 	}
@@ -120,7 +134,6 @@ function BlockPopover( {
 	// position in the right corner.
 	// To do: refactor `Popover` to make this prop clearer.
 	const popoverPosition = showEmptyBlockSideInserter ? 'top left right' : 'top right left';
-	const popoverIsSticky = hasMultiSelection ? '.wp-block.is-multi-selected' : true;
 
 	return (
 		<Popover
@@ -128,9 +141,9 @@ function BlockPopover( {
 			animate={ false }
 			position={ popoverPosition }
 			focusOnMount={ false }
-			anchorRef={ node }
+			anchorRef={ anchorRef }
 			className="block-editor-block-list__block-popover"
-			__unstableSticky={ showEmptyBlockSideInserter ? false : popoverIsSticky }
+			__unstableSticky={ ! showEmptyBlockSideInserter }
 			__unstableSlotName="block-toolbar"
 			// Allow subpixel positioning for the block movement animation.
 			__unstableAllowVerticalSubpixelPosition={ moverDirection !== 'horizontal' && node }
diff --git a/packages/block-editor/src/components/block-list/block.js b/packages/block-editor/src/components/block-list/block.js
index 65b418b243ea42..a78d7af1d5bf2a 100644
--- a/packages/block-editor/src/components/block-list/block.js
+++ b/packages/block-editor/src/components/block-list/block.js
@@ -2,7 +2,7 @@
  * External dependencies
  */
 import classnames from 'classnames';
-import { first, last } from 'lodash';
+import { first, last, omit } from 'lodash';
 import { animated } from 'react-spring/web.cjs';
 
 /**
@@ -42,7 +42,7 @@ import BlockCrashBoundary from './block-crash-boundary';
 import BlockHtml from './block-html';
 import { isInsideRootBlock } from '../../utils/dom';
 import useMovingAnimation from './moving-animation';
-import { Context, SelectedBlockNode } from './root-container';
+import { Context, BlockNodes } from './root-container';
 
 function BlockListBlock( {
 	mode,
@@ -53,6 +53,7 @@ function BlockListBlock( {
 	isMultiSelected,
 	isPartOfMultiSelection,
 	isFirstMultiSelected,
+	isLastMultiSelected,
 	isTypingWithinBlock,
 	isEmptyDefaultBlock,
 	isAncestorOfSelectedBlock,
@@ -77,7 +78,7 @@ function BlockListBlock( {
 	hasSelectedUI = true,
 } ) {
 	const onSelectionStart = useContext( Context );
-	const [ , setSelectedBlockNode ] = useContext( SelectedBlockNode );
+	const [ , setBlockNodes ] = useContext( BlockNodes );
 	// In addition to withSelect, we should favor using useSelect in this component going forward
 	// to avoid leaking new props to the public API (editor.BlockListBlock filter)
 	const { isDraggingBlocks } = useSelect( ( select ) => {
@@ -90,14 +91,14 @@ function BlockListBlock( {
 	const wrapper = useRef( null );
 
 	useLayoutEffect( () => {
-		if ( isSelected || isFirstMultiSelected ) {
+		if ( isSelected || isFirstMultiSelected || isLastMultiSelected ) {
 			const node = wrapper.current;
-			setSelectedBlockNode( node );
+			setBlockNodes( ( nodes ) => ( { ...nodes, [ clientId ]: node } ) );
 			return () => {
-				setSelectedBlockNode( ( n ) => n === node ? null : n );
+				setBlockNodes( ( nodes ) => omit( nodes, clientId ) );
 			};
 		}
-	}, [ isSelected, isFirstMultiSelected ] );
+	}, [ isSelected, isFirstMultiSelected, isLastMultiSelected ] );
 
 	// Handling the error state
 	const [ hasError, setErrorState ] = useState( false );
@@ -332,6 +333,7 @@ const applyWithSelect = withSelect(
 			isAncestorMultiSelected,
 			isBlockMultiSelected,
 			isFirstMultiSelectedBlock,
+			getLastMultiSelectedBlockClientId,
 			isTyping,
 			getBlockMode,
 			isSelectionEnabled,
@@ -362,6 +364,7 @@ const applyWithSelect = withSelect(
 			isPartOfMultiSelection:
 				isBlockMultiSelected( clientId ) || isAncestorMultiSelected( clientId ),
 			isFirstMultiSelected: isFirstMultiSelectedBlock( clientId ),
+			isLastMultiSelected: getLastMultiSelectedBlockClientId() === clientId,
 
 			// We only care about this prop when the block is selected
 			// Thus to avoid unnecessary rerenders we avoid updating the prop if the block is not selected.
diff --git a/packages/block-editor/src/components/block-list/root-container.js b/packages/block-editor/src/components/block-list/root-container.js
index aae8c476c418b5..84985f8fd7c072 100644
--- a/packages/block-editor/src/components/block-list/root-container.js
+++ b/packages/block-editor/src/components/block-list/root-container.js
@@ -15,7 +15,7 @@ import BlockPopover from './block-popover';
 /** @typedef {import('@wordpress/element').WPSyntheticEvent} WPSyntheticEvent */
 
 export const Context = createContext();
-export const SelectedBlockNode = createContext();
+export const BlockNodes = createContext();
 
 function selector( select ) {
 	const {
@@ -81,7 +81,7 @@ function RootContainer( { children, className }, ref ) {
 			selectedBlockClientId={ selectedBlockClientId }
 			containerRef={ ref }
 		>
-			<SelectedBlockNode.Provider value={ useState( null ) }>
+			<BlockNodes.Provider value={ useState( {} ) }>
 				<BlockPopover />
 				<div
 					ref={ ref }
@@ -93,7 +93,7 @@ function RootContainer( { children, className }, ref ) {
 						{ children }
 					</Context.Provider>
 				</div>
-			</SelectedBlockNode.Provider>
+			</BlockNodes.Provider>
 		</InsertionPoint>
 	);
 }
diff --git a/packages/components/src/popover/index.js b/packages/components/src/popover/index.js
index 82cb3874db2fb3..a97c964e065972 100644
--- a/packages/components/src/popover/index.js
+++ b/packages/components/src/popover/index.js
@@ -62,7 +62,25 @@ function computeAnchorRect(
 			return getRectangleFromRange( anchorRef );
 		}
 
-		const rect = anchorRef.getBoundingClientRect();
+		if ( anchorRef instanceof window.Element ) {
+			const rect = anchorRef.getBoundingClientRect();
+
+			if ( shouldAnchorIncludePadding ) {
+				return rect;
+			}
+
+			return withoutPadding( rect, anchorRef );
+		}
+
+		const { top, bottom } = anchorRef;
+		const topRect = top.getBoundingClientRect();
+		const bottomRect = bottom.getBoundingClientRect();
+		const rect = new window.DOMRect(
+			topRect.left,
+			topRect.top,
+			topRect.width,
+			bottomRect.bottom - topRect.top
+		);
 
 		if ( shouldAnchorIncludePadding ) {
 			return rect;
@@ -301,7 +319,7 @@ const Popover = ( {
 				yAxis,
 				contentHeight,
 				contentWidth,
-			} = computePopoverPosition( anchor, contentRect.current, position, __unstableSticky, anchorRef, relativeOffsetTop );
+			} = computePopoverPosition( anchor, contentRect.current, position, __unstableSticky, containerRef.current, relativeOffsetTop );
 
 			if ( typeof popoverTop === 'number' && typeof popoverLeft === 'number' ) {
 				if ( subpixels && __unstableAllowVerticalSubpixelPosition ) {
diff --git a/packages/components/src/popover/utils.js b/packages/components/src/popover/utils.js
index f729247c98d7f5..187f3c292a5642 100644
--- a/packages/components/src/popover/utils.js
+++ b/packages/components/src/popover/utils.js
@@ -128,27 +128,13 @@ export function computePopoverYAxisPosition( anchorRect, contentSize, yAxis, cor
 	const { height } = contentSize;
 
 	if ( sticky ) {
-		let topEl = anchorRef;
-		let bottomEl = anchorRef;
-
-		if ( typeof sticky === 'string' ) {
-			const elements = document.querySelectorAll( sticky );
-
-			if ( elements.length ) {
-				topEl = elements[ 0 ];
-				bottomEl = elements[ elements.length - 1 ];
-			}
-		}
-
-		const scrollContainerEl = getScrollContainer( topEl ) || document.body;
+		const scrollContainerEl = getScrollContainer( anchorRef ) || document.body;
 		const scrollRect = scrollContainerEl.getBoundingClientRect();
-		const topRect = topEl.getBoundingClientRect();
-		const bottomRect = bottomEl.getBoundingClientRect();
 
-		if ( topRect.top - height <= scrollRect.top ) {
+		if ( anchorRect.top - height <= scrollRect.top ) {
 			return {
 				yAxis,
-				popoverTop: Math.min( bottomRect.bottom - relativeOffsetTop, scrollRect.top + height - relativeOffsetTop ),
+				popoverTop: Math.min( anchorRect.bottom - relativeOffsetTop, scrollRect.top + height - relativeOffsetTop ),
 			};
 		}
 	}