diff --git a/packages/block-editor/src/store/private-selectors.js b/packages/block-editor/src/store/private-selectors.js
index c46778d889b3e0..b02f7e67bd6134 100644
--- a/packages/block-editor/src/store/private-selectors.js
+++ b/packages/block-editor/src/store/private-selectors.js
@@ -17,6 +17,8 @@ import {
 	getClientIdsWithDescendants,
 	isNavigationMode,
 	getBlockRootClientId,
+	getBlocksByName,
+	getBlockAttributes,
 } from './selectors';
 import {
 	checkAllowListRecursive,
@@ -563,10 +565,24 @@ export const getBlockStyles = createSelector(
  *
  * @param {Object} state Editor state.
  *
- * @return {string|undefined} The section root client ID or undefined if not set.
+ * @return {string} The section root client ID.
  */
 export function getSectionRootClientId( state ) {
-	return state.settings?.[ sectionRootClientIdKey ];
+	const settingsRootClientId = state.settings?.[ sectionRootClientIdKey ];
+
+	// Specifically check that the setting was not provided to avoid
+	// cases where the provided setting is an empty string to signify
+	// the "root block" of the editor.
+	if ( settingsRootClientId !== undefined ) {
+		return settingsRootClientId;
+	}
+
+	return (
+		getBlocksByName( state, 'core/group' ).find(
+			( clientId ) =>
+				getBlockAttributes( state, clientId )?.tagName === 'main'
+		) ?? ''
+	);
 }
 
 /**
diff --git a/packages/editor/src/components/provider/use-block-editor-settings.js b/packages/editor/src/components/provider/use-block-editor-settings.js
index f5c45f431e2c85..b9b09d01ccaf4c 100644
--- a/packages/editor/src/components/provider/use-block-editor-settings.js
+++ b/packages/editor/src/components/provider/use-block-editor-settings.js
@@ -133,8 +133,7 @@ function useBlockEditorSettings( settings, postType, postId, renderingMode ) {
 			} = select( coreStore );
 			const { get } = select( preferencesStore );
 			const { getBlockTypes } = select( blocksStore );
-			const { getBlocksByName, getBlockAttributes } =
-				select( blockEditorStore );
+			const { getBlocksByName } = select( blockEditorStore );
 			const siteSettings = canUser( 'read', {
 				kind: 'root',
 				name: 'site',
@@ -144,15 +143,11 @@ function useBlockEditorSettings( settings, postType, postId, renderingMode ) {
 
 			function getSectionRootBlock() {
 				if ( renderingMode === 'template-locked' ) {
-					return getBlocksByName( 'core/post-content' )?.[ 0 ] ?? '';
+					return getBlocksByName( 'core/post-content' )?.[ 0 ] ?? ''
 				}
 
-				return (
-					getBlocksByName( 'core/group' ).find(
-						( clientId ) =>
-							getBlockAttributes( clientId )?.tagName === 'main'
-					) ?? ''
-				);
+				// Allow default algorithm to determine the section root block.
+				return undefined;
 			}
 
 			return {