diff --git a/packages/block-editor/src/components/block-inspector/index.js b/packages/block-editor/src/components/block-inspector/index.js
index 475d4f6a4b8c2e..5648cc2c6370f9 100644
--- a/packages/block-editor/src/components/block-inspector/index.js
+++ b/packages/block-editor/src/components/block-inspector/index.js
@@ -29,8 +29,10 @@ import useBlockInspectorAnimationSettings from './useBlockInspectorAnimationSett
 import BlockInfo from '../block-info-slot-fill';
 import BlockQuickNavigation from '../block-quick-navigation';
 import { useBorderPanelLabel } from '../../hooks/border';
+import { privateApis as blockEditorPrivateApis } from '../../private-apis';
 
 import { unlock } from '../../lock-unlock';
+const { PrivateListView } = unlock( blockEditorPrivateApis );
 
 function BlockStylesPanel( { clientId } ) {
 	return (
@@ -213,6 +215,7 @@ const BlockInspectorSingleBlock = ( {
 	isSectionBlock,
 } ) => {
 	const availableTabs = useInspectorControlsTabs( blockName );
+
 	const showTabs = ! isSectionBlock && availableTabs?.length > 1;
 
 	const hasBlockStyles = useSelect(
@@ -223,6 +226,7 @@ const BlockInspectorSingleBlock = ( {
 		},
 		[ blockName ]
 	);
+
 	const blockInformation = useBlockDisplayInformation( clientId );
 	const borderPanelLabel = useBorderPanelLabel( { blockName } );
 	const contentClientIds = useSelect(
@@ -246,6 +250,41 @@ const BlockInspectorSingleBlock = ( {
 		[ isSectionBlock, clientId ]
 	);
 
+	const {
+		selectedContentClientId,
+		isSelectedContentClientIdControlling,
+		isSelectedBlockInContentOnlyContainer,
+	} = useSelect( ( select ) => {
+		const {
+			getSelectedBlockClientId,
+			areInnerBlocksControlled,
+			getBlockRootClientId,
+			getTemplateLock,
+		} = select( blockEditorStore );
+
+		const _selectedBlockClientId = getSelectedBlockClientId();
+		const _isSelectedContentClientIdControlling = areInnerBlocksControlled(
+			_selectedBlockClientId
+		);
+
+		const rootClientId = getBlockRootClientId( _selectedBlockClientId );
+		const templateLock = getTemplateLock( rootClientId );
+
+		const _isSelectedBlockInContentOnlyContainer =
+			templateLock === 'contentOnly';
+
+		return {
+			selectedContentClientId: _selectedBlockClientId,
+			isSelectedContentClientIdControlling:
+				_isSelectedContentClientIdControlling,
+			isSelectedBlockInContentOnlyContainer:
+				_isSelectedBlockInContentOnlyContainer,
+			hasContentLockedParent: false,
+		};
+	} );
+	const { __unstableGetEditorMode } = useSelect( blockEditorStore );
+	const editorMode = __unstableGetEditorMode();
+
 	return (
 		<div className="block-editor-block-inspector">
 			<BlockCard
@@ -268,16 +307,48 @@ const BlockInspectorSingleBlock = ( {
 						<BlockStylesPanel clientId={ clientId } />
 					) }
 
-					{ contentClientIds && contentClientIds?.length > 0 && (
-						<PanelBody title={ __( 'Content' ) }>
-							<BlockQuickNavigation
-								clientIds={ contentClientIds }
-							/>
-						</PanelBody>
-					) }
+					{ ! isSelectedContentClientIdControlling &&
+						contentClientIds &&
+						contentClientIds?.length > 0 && (
+							<PanelBody title={ __( 'Content' ) }>
+								<BlockQuickNavigation
+									clientIds={ contentClientIds }
+								/>
+							</PanelBody>
+						) }
+
+					{ isSelectedContentClientIdControlling &&
+						isSelectedBlockInContentOnlyContainer &&
+						contentClientIds &&
+						contentClientIds?.length > 0 && (
+							<PanelBody title={ __( 'Content' ) }>
+								<PrivateListView
+									rootClientId={ selectedContentClientId }
+									ignoreRenderingMode
+									isExpanded
+									description={ __( 'Inner blocks' ) }
+									showAppender={ false }
+								/>
+							</PanelBody>
+						) }
 
 					{ ! isSectionBlock && (
 						<>
+							{ editorMode === 'navigation' &&
+								isSelectedBlockInContentOnlyContainer &&
+								isSelectedContentClientIdControlling && (
+									<PanelBody title={ __( 'Content' ) }>
+										<PrivateListView
+											rootClientId={
+												selectedContentClientId
+											}
+											ignoreRenderingMode
+											isExpanded
+											description={ __( 'Inner blocks' ) }
+											showAppender={ false }
+										/>
+									</PanelBody>
+								) }
 							<InspectorControls.Slot />
 							<InspectorControls.Slot group="list" />
 							<InspectorControls.Slot
diff --git a/packages/block-editor/src/components/list-view/index.js b/packages/block-editor/src/components/list-view/index.js
index d7961bd6c02f3d..a2b7ff80f072ab 100644
--- a/packages/block-editor/src/components/list-view/index.js
+++ b/packages/block-editor/src/components/list-view/index.js
@@ -78,6 +78,7 @@ export const BLOCK_LIST_ITEM_HEIGHT = 32;
  * @param {?HTMLElement}   props.dropZoneElement        Optional element to be used as the drop zone.
  * @param {?boolean}       props.showBlockMovers        Flag to enable block movers. Defaults to `false`.
  * @param {?boolean}       props.isExpanded             Flag to determine whether nested levels are expanded by default. Defaults to `false`.
+ * @param {?boolean}       props.ignoreRenderingMode    Flag to ignore rendering mode and always show the block. Defaults to `false`.
  * @param {?boolean}       props.showAppender           Flag to show or hide the block appender. Defaults to `false`.
  * @param {?ComponentType} props.blockSettingsMenu      Optional more menu substitution. Defaults to the standard `BlockSettingsDropdown` component.
  * @param {string}         props.rootClientId           The client id of the root block from which we determine the blocks to show in the list.
@@ -93,6 +94,7 @@ function ListViewComponent(
 		dropZoneElement,
 		showBlockMovers = false,
 		isExpanded = false,
+		ignoreRenderingMode = false,
 		showAppender = false,
 		blockSettingsMenu: BlockSettingsMenu = BlockSettingsDropdown,
 		rootClientId,
@@ -115,7 +117,7 @@ function ListViewComponent(
 
 	const instanceId = useInstanceId( ListViewComponent );
 	const { clientIdsTree, draggedClientIds, selectedClientIds } =
-		useListViewClientIds( { blocks, rootClientId } );
+		useListViewClientIds( { blocks, rootClientId, ignoreRenderingMode } );
 	const blockIndexes = useListViewBlockIndexes( clientIdsTree );
 
 	const { getBlock } = useSelect( blockEditorStore );
diff --git a/packages/block-editor/src/components/list-view/use-list-view-client-ids.js b/packages/block-editor/src/components/list-view/use-list-view-client-ids.js
index 8a1ccfcede4c12..0980818b418280 100644
--- a/packages/block-editor/src/components/list-view/use-list-view-client-ids.js
+++ b/packages/block-editor/src/components/list-view/use-list-view-client-ids.js
@@ -10,22 +10,29 @@ import { useSelect } from '@wordpress/data';
 import { store as blockEditorStore } from '../../store';
 import { unlock } from '../../lock-unlock';
 
-export default function useListViewClientIds( { blocks, rootClientId } ) {
+export default function useListViewClientIds( {
+	blocks,
+	rootClientId,
+	ignoreRenderingMode,
+} ) {
 	return useSelect(
 		( select ) => {
 			const {
 				getDraggedBlockClientIds,
 				getSelectedBlockClientIds,
 				getEnabledClientIdsTree,
+				__unstableGetClientIdsTree: getClientIdsTree,
 			} = unlock( select( blockEditorStore ) );
 
 			return {
 				selectedClientIds: getSelectedBlockClientIds(),
 				draggedClientIds: getDraggedBlockClientIds(),
 				clientIdsTree:
-					blocks ?? getEnabledClientIdsTree( rootClientId ),
+					blocks ?? ignoreRenderingMode
+						? getClientIdsTree( rootClientId )
+						: getEnabledClientIdsTree( rootClientId ),
 			};
 		},
-		[ blocks, rootClientId ]
+		[ blocks, rootClientId, ignoreRenderingMode ]
 	);
 }
diff --git a/packages/block-editor/src/store/private-selectors.js b/packages/block-editor/src/store/private-selectors.js
index f1b5abd7789a11..d8fbb87e6c12f6 100644
--- a/packages/block-editor/src/store/private-selectors.js
+++ b/packages/block-editor/src/store/private-selectors.js
@@ -90,6 +90,7 @@ function getEnabledClientIdsTreeUnmemoized( state, rootClientId ) {
 			state,
 			clientId
 		);
+
 		if ( getBlockEditingMode( state, clientId ) !== 'disabled' ) {
 			result.push( { clientId, innerBlocks } );
 		} else {
diff --git a/packages/block-editor/src/store/selectors.js b/packages/block-editor/src/store/selectors.js
index 598b6b4ea480de..fb59a55e9b114c 100644
--- a/packages/block-editor/src/store/selectors.js
+++ b/packages/block-editor/src/store/selectors.js
@@ -3068,6 +3068,12 @@ export const getBlockEditingMode = createRegistrySelector(
 					return 'contentOnly';
 				}
 
+				// All controlling blocks are treated as content only
+				// by default.
+				if ( areInnerBlocksControlled( state, clientId ) ) {
+					return 'contentOnly';
+				}
+
 				return 'disabled';
 			}
 
@@ -3107,6 +3113,15 @@ export const getBlockEditingMode = createRegistrySelector(
 				);
 				const isContent = hasContentRoleAttribute( name );
 
+				// All controlling blocks are treated as content only
+				// by default.
+				if (
+					! isContent &&
+					areInnerBlocksControlled( state, clientId )
+				) {
+					return 'contentOnly';
+				}
+
 				return isContent ? 'contentOnly' : 'disabled';
 			}
 
@@ -3130,6 +3145,16 @@ export const getBlockEditingMode = createRegistrySelector(
 					select( blocksStore )
 				);
 				const isContent = hasContentRoleAttribute( name );
+
+				// All controlling blocks are treated as content only
+				// by default.
+				if (
+					! isContent &&
+					areInnerBlocksControlled( state, clientId )
+				) {
+					return 'contentOnly';
+				}
+
 				return isContent ? 'contentOnly' : 'disabled';
 			}
 			// Otherwise, check if there's an ancestor that is contentOnly
diff --git a/packages/block-library/src/navigation/edit/inner-blocks.js b/packages/block-library/src/navigation/edit/inner-blocks.js
index 6fe3dd8347a33e..e2534a20ed1bb5 100644
--- a/packages/block-library/src/navigation/edit/inner-blocks.js
+++ b/packages/block-library/src/navigation/edit/inner-blocks.js
@@ -73,6 +73,11 @@ export default function NavigationInnerBlocks( {
 	const showPlaceholder =
 		! hasCustomPlaceholder && ! hasMenuItems && ! isSelected;
 
+	const defaultRenderingMode = useSelect( ( select ) => {
+		const { getBlockEditingMode } = select( blockEditorStore );
+		return getBlockEditingMode( clientId ) === 'default';
+	} );
+
 	const innerBlocksProps = useInnerBlocksProps(
 		{
 			className: 'wp-block-navigation__container',
@@ -93,13 +98,14 @@ export default function NavigationInnerBlocks( {
 			// the sibling inserter.
 			// See https://github.com/WordPress/gutenberg/issues/37572.
 			renderAppender:
-				isSelected ||
+				defaultRenderingMode &&
+				( isSelected ||
 				( isImmediateParentOfSelectedBlock &&
 					! selectedBlockHasChildren ) ||
 				// Show the appender while dragging to allow inserting element between item and the appender.
 				parentOrChildHasSelection
 					? InnerBlocks.ButtonBlockAppender
-					: false,
+					: false ),
 			placeholder: showPlaceholder ? placeholder : undefined,
 			__experimentalCaptureToolbars: true,
 			__unstableDisableLayoutClassNames: true,