diff --git a/packages/edit-post/src/components/layout/index.js b/packages/edit-post/src/components/layout/index.js
index 185f97ba45a56..2cbf5c32e814b 100644
--- a/packages/edit-post/src/components/layout/index.js
+++ b/packages/edit-post/src/components/layout/index.js
@@ -24,7 +24,12 @@ import {
 } from '@wordpress/block-editor';
 import { PluginArea } from '@wordpress/plugins';
 import { __, sprintf } from '@wordpress/i18n';
-import { useCallback, useMemo } from '@wordpress/element';
+import {
+	useCallback,
+	useLayoutEffect,
+	useMemo,
+	useRef,
+} from '@wordpress/element';
 import { store as noticesStore } from '@wordpress/notices';
 import { store as preferencesStore } from '@wordpress/preferences';
 import {
@@ -36,8 +41,8 @@ import { privateApis as blockLibraryPrivateApis } from '@wordpress/block-library
 import { addQueryArgs } from '@wordpress/url';
 import { decodeEntities } from '@wordpress/html-entities';
 import { store as coreStore } from '@wordpress/core-data';
-import { SlotFillProvider } from '@wordpress/components';
-import { useViewportMatch } from '@wordpress/compose';
+import { ResizableBox, SlotFillProvider } from '@wordpress/components';
+import { useMediaQuery, useViewportMatch } from '@wordpress/compose';
 
 /**
  * Internal dependencies
@@ -151,6 +156,118 @@ function useEditorStyles() {
 	] );
 }
 
+/**
+ * @param {Object}  props
+ * @param {boolean} props.isLegacy True when the editor canvas is not in an iframe.
+ */
+function MetaBoxesMain( { isLegacy } ) {
+	const [ isOpen, openHeight, hasAnyVisible ] = useSelect( ( select ) => {
+		const { get } = select( preferencesStore );
+		const { isMetaBoxLocationVisible } = select( editPostStore );
+		return [
+			get( 'core/edit-post', 'metaBoxesMainIsOpen' ),
+			get( 'core/edit-post', 'metaBoxesMainOpenHeight' ),
+			isMetaBoxLocationVisible( 'normal' ) ||
+				isMetaBoxLocationVisible( 'advanced' ) ||
+				isMetaBoxLocationVisible( 'side' ),
+		];
+	}, [] );
+	const { set: setPreference } = useDispatch( preferencesStore );
+	const resizableBoxRef = useRef();
+	const isShort = useMediaQuery( '(max-height: 549px)' );
+
+	const isAutoHeight = openHeight === undefined;
+	// In case a user size is set stops the default max-height from applying.
+	useLayoutEffect( () => {
+		if ( ! isLegacy && hasAnyVisible && ! isShort && ! isAutoHeight ) {
+			resizableBoxRef.current.resizable.classList.add( 'has-user-size' );
+		}
+	}, [ isAutoHeight, isShort, hasAnyVisible, isLegacy ] );
+
+	if ( ! hasAnyVisible ) {
+		return;
+	}
+
+	const className = 'edit-post-meta-boxes-main';
+	const contents = (
+		<div
+			className={ clsx(
+				// The class name 'edit-post-layout__metaboxes' is retained because some plugins use it.
+				'edit-post-layout__metaboxes',
+				! isLegacy && 'edit-post-meta-boxes-main__liner'
+			) }
+		>
+			<MetaBoxes location="normal" />
+			<MetaBoxes location="advanced" />
+		</div>
+	);
+
+	if ( isLegacy ) {
+		return contents;
+	}
+
+	if ( isShort ) {
+		return (
+			<details
+				className={ className }
+				open={ isOpen }
+				onToggle={ ( { target } ) => {
+					setPreference(
+						'core/edit-post',
+						'metaBoxesMainIsOpen',
+						target.open
+					);
+				} }
+			>
+				<summary>{ __( 'Meta Boxes' ) }</summary>
+				{ contents }
+			</details>
+		);
+	}
+	return (
+		<ResizableBox
+			className={ className }
+			defaultSize={ { height: openHeight } }
+			ref={ resizableBoxRef }
+			enable={ {
+				top: true,
+				right: false,
+				bottom: false,
+				left: false,
+				topLeft: false,
+				topRight: false,
+				bottomRight: false,
+				bottomLeft: false,
+			} }
+			// This is overriden by an !important rule that applies until user resizes.
+			maxHeight="100%"
+			bounds="parent"
+			boundsByDirection
+			// Avoids hiccups while dragging over objects like iframes and ensures that
+			// the event to end the drag is captured by the target (resize handle)
+			// whether or not it’s under the pointer.
+			onPointerDown={ ( { pointerId, target } ) => {
+				target.setPointerCapture( pointerId );
+			} }
+			onResizeStart={ ( event, direction, elementRef ) => {
+				// Avoids height jumping in case it’s limited by max-height.
+				elementRef.style.height = `${ elementRef.offsetHeight }px`;
+				// Stops initial max-height from being applied.
+				elementRef.classList.add( 'has-user-size' );
+			} }
+			onResizeStop={ () => {
+				setPreference(
+					'core/edit-post',
+					'metaBoxesMainOpenHeight',
+					resizableBoxRef.current.state.height
+				);
+			} }
+		>
+			{ contents }
+		</ResizableBox>
+	);
+}
+
 function Layout( {
 	postId: initialPostId,
 	postType: initialPostType,
@@ -355,10 +472,7 @@ function Layout( {
 					extraContent={
 						! isDistractionFree &&
 						showMetaBoxes && (
-							<div className="edit-post-layout__metaboxes">
-								<MetaBoxes location="normal" />
-								<MetaBoxes location="advanced" />
-							</div>
+							<MetaBoxesMain isLegacy={ ! shouldIframe } />
 						)
 					}
 				>
diff --git a/packages/edit-post/src/components/layout/style.scss b/packages/edit-post/src/components/layout/style.scss
index 5fdaceaa002be..5392a7e9da4d9 100644
--- a/packages/edit-post/src/components/layout/style.scss
+++ b/packages/edit-post/src/components/layout/style.scss
@@ -1,6 +1,70 @@
-.edit-post-layout__metaboxes {
-	flex-shrink: 0;
-	clear: both;
+.edit-post-meta-boxes-main {
+	filter: drop-shadow(0 -1px rgba($color: #000, $alpha: 0.133)); // 0.133 = $gray-200 but with alpha.
+	background-color: $white;
+	clear: both; // This is seemingly only needed in case the canvas is not iframe’d.
+
+	&:not(details) {
+		padding-top: 23px;
+		max-height: 100%;
+
+		&:not(.has-user-size) {
+			max-height: 50% !important;
+		}
+	}
+
+	// The component renders as a details element in short viewports.
+	&:is(details) {
+		& > summary {
+			cursor: pointer;
+			color: $gray-900;
+			background-color: $white;
+			height: $button-size-compact;
+			line-height: $button-size-compact;
+			font-size: 13px;
+			padding-left: $grid-unit-30;
+			box-shadow: 0 $border-width $gray-300;
+		}
+
+		&[open] > summary {
+			position: sticky;
+			top: 0;
+			z-index: 1;
+		}
+	}
+
+	& .components-resizable-box__handle-top {
+		top: 0;
+		box-shadow: 0 $border-width $gray-300;
+	}
+	& .components-resizable-box__side-handle::before {
+		border-radius: 0;
+		top: 0;
+		height: $border-width;
+	}
+	& .components-resizable-box__handle::after {
+		background-color: $gray-300;
+		box-shadow: none;
+		border-radius: 4px;
+		height: $grid-unit-05;
+		top: calc(50% - #{$grid-unit-05} / 2);
+		width: 100px;
+		right: calc(50% - 50px);
+	}
+}
+
+.edit-post-meta-boxes-main__liner {
+	overflow: auto;
+	max-height: 100%;
+	// Keep the contents behind the resize handle or details summary.
+	isolation: isolate;
+}
+
+.has-metaboxes .editor-visual-editor {
+	flex: 1;
+
+	&.is-iframed {
+		isolation: isolate;
+	}
 }
 
 // Adjust the position of the notices
diff --git a/packages/edit-post/src/components/layout/use-should-iframe.js b/packages/edit-post/src/components/layout/use-should-iframe.js
index 248ea53109f25..e36a4773c4a1f 100644
--- a/packages/edit-post/src/components/layout/use-should-iframe.js
+++ b/packages/edit-post/src/components/layout/use-should-iframe.js
@@ -6,11 +6,6 @@ import { useSelect } from '@wordpress/data';
 import { store as blocksStore } from '@wordpress/blocks';
 import { store as blockEditorStore } from '@wordpress/block-editor';
 
-/**
- * Internal dependencies
- */
-import { store as editPostStore } from '../../store';
-
 const isGutenbergPlugin = globalThis.IS_GUTENBERG_PLUGIN ? true : false;
 
 export function useShouldIframe() {
@@ -18,7 +13,6 @@ export function useShouldIframe() {
 		isBlockBasedTheme,
 		hasV3BlocksOnly,
 		isEditingTemplate,
-		hasMetaBoxes,
 		isZoomOutMode,
 	} = useSelect( ( select ) => {
 		const { getEditorSettings, getCurrentPostType } = select( editorStore );
@@ -31,14 +25,13 @@ export function useShouldIframe() {
 				return type.apiVersion >= 3;
 			} ),
 			isEditingTemplate: getCurrentPostType() === 'wp_template',
-			hasMetaBoxes: select( editPostStore ).hasMetaBoxes(),
 			isZoomOutMode: __unstableGetEditorMode() === 'zoom-out',
 		};
 	}, [] );
 
 	return (
-		( ( hasV3BlocksOnly || ( isGutenbergPlugin && isBlockBasedTheme ) ) &&
-			! hasMetaBoxes ) ||
+		hasV3BlocksOnly ||
+		( isGutenbergPlugin && isBlockBasedTheme ) ||
 		isEditingTemplate ||
 		isZoomOutMode
 	);
diff --git a/packages/edit-post/src/store/selectors.js b/packages/edit-post/src/store/selectors.js
index da1f9959e32e9..5bea6e7d35eb6 100644
--- a/packages/edit-post/src/store/selectors.js
+++ b/packages/edit-post/src/store/selectors.js
@@ -379,7 +379,6 @@ export const isMetaBoxLocationVisible = createRegistrySelector(
 			isMetaBoxLocationActive( state, location ) &&
 			getMetaBoxesPerLocation( state, location )?.some( ( { id } ) => {
 				return select( editorStore ).isEditorPanelEnabled(
-					state,
 					`meta-box-${ id }`
 				);
 			} )
diff --git a/test/e2e/specs/editor/plugins/meta-boxes.spec.js b/test/e2e/specs/editor/plugins/meta-boxes.spec.js
index 1b7adc18760ff..511b3837f8030 100644
--- a/test/e2e/specs/editor/plugins/meta-boxes.spec.js
+++ b/test/e2e/specs/editor/plugins/meta-boxes.spec.js
@@ -26,7 +26,7 @@ test.describe( 'Meta boxes', () => {
 		await expect( saveDraft ).toBeDisabled();
 
 		// Add title to enable valid non-empty post save.
-		await page
+		await editor.canvas
 			.getByRole( 'textbox', { name: 'Add title' } )
 			.fill( 'Hello Meta' );
 
@@ -44,7 +44,7 @@ test.describe( 'Meta boxes', () => {
 		page,
 	} ) => {
 		// Publish a post so there's something for the latest posts dynamic block to render.
-		await page
+		await editor.canvas
 			.getByRole( 'textbox', { name: 'Add title' } )
 			.fill( 'A published post' );
 		await page.keyboard.press( 'Enter' );
@@ -53,7 +53,7 @@ test.describe( 'Meta boxes', () => {
 
 		// Publish a post with the latest posts dynamic block.
 		await admin.createNewPost();
-		await page
+		await editor.canvas
 			.getByRole( 'textbox', { name: 'Add title' } )
 			.fill( 'Dynamic block test' );
 		await editor.insertBlock( { name: 'core/latest-posts' } );
@@ -70,10 +70,12 @@ test.describe( 'Meta boxes', () => {
 		editor,
 		page,
 	} ) => {
-		await page
+		await editor.canvas
 			.getByRole( 'textbox', { name: 'Add title' } )
 			.fill( 'A published post' );
-		await page.getByRole( 'button', { name: 'Add default block' } ).click();
+		await editor.canvas
+			.getByRole( 'button', { name: 'Add default block' } )
+			.click();
 		await page.keyboard.type( 'Excerpt from content.' );
 
 		const postId = await editor.publishPost();
@@ -89,9 +91,11 @@ test.describe( 'Meta boxes', () => {
 		page,
 	} ) => {
 		await editor.openDocumentSettingsSidebar();
-		await page.getByRole( 'button', { name: 'Add default block' } ).click();
+		await editor.canvas
+			.getByRole( 'button', { name: 'Add default block' } )
+			.click();
 		await page.keyboard.type( 'Excerpt from content.' );
-		await page
+		await editor.canvas
 			.getByRole( 'textbox', { name: 'Add title' } )
 			.fill( 'A published post' );
 
diff --git a/test/e2e/specs/editor/plugins/wp-editor-meta-box.spec.js b/test/e2e/specs/editor/plugins/wp-editor-meta-box.spec.js
index 710e06b35e124..c5eafdafe918d 100644
--- a/test/e2e/specs/editor/plugins/wp-editor-meta-box.spec.js
+++ b/test/e2e/specs/editor/plugins/wp-editor-meta-box.spec.js
@@ -20,7 +20,7 @@ test.describe( 'WP Editor Meta Boxes', () => {
 		await admin.createNewPost();
 
 		// Add title to enable valid non-empty post save.
-		await page
+		await editor.canvas
 			.locator( 'role=textbox[name="Add title"i]' )
 			.type( 'Hello Meta' );
 
diff --git a/test/e2e/specs/editor/various/publish-button.spec.js b/test/e2e/specs/editor/various/publish-button.spec.js
index 631ddcd0fe61b..cdc9c1a993636 100644
--- a/test/e2e/specs/editor/various/publish-button.spec.js
+++ b/test/e2e/specs/editor/various/publish-button.spec.js
@@ -70,13 +70,12 @@ test.describe( 'Post publish button', () => {
 		admin,
 		page,
 		requestUtils,
+		editor,
 	} ) => {
 		await requestUtils.activatePlugin( 'gutenberg-test-plugin-meta-box' );
 		await admin.createNewPost();
-		await page
-			.getByRole( 'textbox', {
-				name: 'Add title',
-			} )
+		await editor.canvas
+			.getByRole( 'textbox', { name: 'Add title' } )
 			.fill( 'Test post' );
 
 		const topBar = page.getByRole( 'region', { name: 'Editor top bar' } );