diff --git a/packages/block-library/src/post-template/index.php b/packages/block-library/src/post-template/index.php
index 9126355c096a5..64cdd156a5431 100644
--- a/packages/block-library/src/post-template/index.php
+++ b/packages/block-library/src/post-template/index.php
@@ -64,6 +64,11 @@ function render_block_core_post_template( $attributes, $content, $block ) {
 		if ( in_the_loop() ) {
 			$query = clone $wp_query;
 			$query->rewind_posts();
+
+			// If in a single post of any post type, default to the 'post' post type.
+			if ( is_singular() ) {
+				query_posts( array( 'post_type' => 'post' ) );
+			}
 		} else {
 			$query = $wp_query;
 		}
diff --git a/packages/block-library/src/query/block.json b/packages/block-library/src/query/block.json
index 9eb8495963823..22bfa7b713801 100644
--- a/packages/block-library/src/query/block.json
+++ b/packages/block-library/src/query/block.json
@@ -41,6 +41,7 @@
 			"default": false
 		}
 	},
+	"usesContext": [ "postType" ],
 	"providesContext": {
 		"queryId": "queryId",
 		"query": "query",
diff --git a/packages/block-library/src/query/edit/inspector-controls/index.js b/packages/block-library/src/query/edit/inspector-controls/index.js
index 6c246ab89b3b3..4085128e9aef1 100644
--- a/packages/block-library/src/query/edit/inspector-controls/index.js
+++ b/packages/block-library/src/query/edit/inspector-controls/index.js
@@ -45,7 +45,7 @@ import { useToolsPanelDropdownMenuProps } from '../../../utils/hooks';
 const { BlockInfo } = unlock( blockEditorPrivateApis );
 
 export default function QueryInspectorControls( props ) {
-	const { attributes, setQuery, setDisplayLayout } = props;
+	const { attributes, setQuery, setDisplayLayout, isTemplate } = props;
 	const { query, displayLayout } = attributes;
 	const {
 		order,
@@ -103,6 +103,7 @@ export default function QueryInspectorControls( props ) {
 		if ( ! hasFormatSupport ) {
 			updateQuery.format = [];
 		}
+
 		setQuery( updateQuery );
 	};
 	const [ querySearch, setQuerySearch ] = useState( query.search );
@@ -118,20 +119,25 @@ export default function QueryInspectorControls( props ) {
 		onChangeDebounced();
 		return onChangeDebounced.cancel;
 	}, [ querySearch, onChangeDebounced ] );
-	const showInheritControl = isControlAllowed( allowedControls, 'inherit' );
+
+	const showInheritControl =
+		isTemplate && isControlAllowed( allowedControls, 'inherit' );
 	const showPostTypeControl =
-		! inherit && isControlAllowed( allowedControls, 'postType' );
+		( ! inherit && isControlAllowed( allowedControls, 'postType' ) ) ||
+		! isTemplate;
 	const postTypeControlLabel = __( 'Post type' );
 	const postTypeControlHelp = __(
 		'Select the type of content to display: posts, pages, or custom post types.'
 	);
 	const showColumnsControl = false;
 	const showOrderControl =
-		! inherit && isControlAllowed( allowedControls, 'order' );
+		( ! inherit && isControlAllowed( allowedControls, 'order' ) ) ||
+		! isTemplate;
 	const showStickyControl =
-		! inherit &&
-		showSticky &&
-		isControlAllowed( allowedControls, 'sticky' );
+		( ! inherit &&
+			showSticky &&
+			isControlAllowed( allowedControls, 'sticky' ) ) ||
+		( showSticky && ! isTemplate );
 	const showSettingsPanel =
 		showInheritControl ||
 		showPostTypeControl ||
diff --git a/packages/block-library/src/query/edit/query-content.js b/packages/block-library/src/query/edit/query-content.js
index 4624b3b96049e..8b3ff09b17934 100644
--- a/packages/block-library/src/query/edit/query-content.js
+++ b/packages/block-library/src/query/edit/query-content.js
@@ -3,7 +3,7 @@
  */
 import { useSelect, useDispatch } from '@wordpress/data';
 import { useInstanceId } from '@wordpress/compose';
-import { useEffect } from '@wordpress/element';
+import { useEffect, useCallback } from '@wordpress/element';
 import {
 	BlockControls,
 	InspectorControls,
@@ -32,6 +32,7 @@ export default function QueryContent( {
 	openPatternSelectionModal,
 	name,
 	clientId,
+	context,
 } ) {
 	const {
 		queryId,
@@ -41,6 +42,7 @@ export default function QueryContent( {
 		tagName: TagName = 'div',
 		query: { inherit } = {},
 	} = attributes;
+	const { postType } = context;
 	const { __unstableMarkNextChangeAsNotPersistent } =
 		useDispatch( blockEditorStore );
 	const instanceId = useInstanceId( QueryContent );
@@ -48,6 +50,16 @@ export default function QueryContent( {
 	const innerBlocksProps = useInnerBlocksProps( blockProps, {
 		template: TEMPLATE,
 	} );
+	const isTemplate = useSelect(
+		( select ) => {
+			const currentTemplate =
+				select( coreStore ).__experimentalGetTemplateForLink()?.type;
+			const isInTemplate = 'wp_template' === currentTemplate;
+			const isInSingularContent = postType !== undefined;
+			return isInTemplate && ! isInSingularContent;
+		},
+		[ postType ]
+	);
 	const { postsPerPage } = useSelect( ( select ) => {
 		const { getSettings } = select( blockEditorStore );
 		const { getEntityRecord, getEntityRecordEdits, canUser } =
@@ -81,6 +93,10 @@ export default function QueryContent( {
 	// Changes in query property (which is an object) need to be in the same callback,
 	// because updates are batched after the render and changes in different query properties
 	// would cause to override previous wanted changes.
+	const updateQuery = useCallback(
+		( newQuery ) => setAttributes( { query: { ...query, ...newQuery } } ),
+		[ query, setAttributes ]
+	);
 	useEffect( () => {
 		const newQuery = {};
 		// When we inherit from global query always need to set the `perPage`
@@ -90,11 +106,24 @@ export default function QueryContent( {
 		} else if ( ! query.perPage && postsPerPage ) {
 			newQuery.perPage = postsPerPage;
 		}
+		// We need to reset the `inherit` value if not in a template, as queries
+		// are not inherited when outside a template (e.g. when in singular content).
+		if ( ! isTemplate && query.inherit ) {
+			newQuery.inherit = false;
+		}
 		if ( !! Object.keys( newQuery ).length ) {
 			__unstableMarkNextChangeAsNotPersistent();
 			updateQuery( newQuery );
 		}
-	}, [ query.perPage, postsPerPage, inherit ] );
+	}, [
+		query.perPage,
+		postsPerPage,
+		inherit,
+		isTemplate,
+		query.inherit,
+		__unstableMarkNextChangeAsNotPersistent,
+		updateQuery,
+	] );
 	// We need this for multi-query block pagination.
 	// Query parameters for each block are scoped to their ID.
 	useEffect( () => {
@@ -102,9 +131,12 @@ export default function QueryContent( {
 			__unstableMarkNextChangeAsNotPersistent();
 			setAttributes( { queryId: instanceId } );
 		}
-	}, [ queryId, instanceId ] );
-	const updateQuery = ( newQuery ) =>
-		setAttributes( { query: { ...query, ...newQuery } } );
+	}, [
+		queryId,
+		instanceId,
+		__unstableMarkNextChangeAsNotPersistent,
+		setAttributes,
+	] );
 	const updateDisplayLayout = ( newDisplayLayout ) =>
 		setAttributes( {
 			displayLayout: { ...displayLayout, ...newDisplayLayout },
@@ -135,6 +167,7 @@ export default function QueryContent( {
 					setDisplayLayout={ updateDisplayLayout }
 					setAttributes={ setAttributes }
 					clientId={ clientId }
+					isTemplate={ isTemplate }
 				/>
 			</InspectorControls>
 			<BlockControls>
diff --git a/phpunit/blocks/render-post-template-test.php b/phpunit/blocks/render-post-template-test.php
index e375758044681..6241f6f060516 100644
--- a/phpunit/blocks/render-post-template-test.php
+++ b/phpunit/blocks/render-post-template-test.php
@@ -113,9 +113,10 @@ public function test_rendering_post_template_with_main_query_loop() {
 	}
 
 	/**
-	 * Tests that the `core/post-template` block does not tamper with the main query loop when rendering within a post
+	 * Tests that the `core/post-template` block does not tamper with the main query loop when rendering within a single post
 	 * as the main query loop has already been started. In this case, the main query object needs to be cloned to
 	 * prevent an infinite loop.
+	 * Also tests that the default query returns posts of the 'post' post type when in a single post of any post type.
 	 */
 	public function test_rendering_post_template_with_main_query_loop_already_started() {
 		global $wp_query, $wp_the_query;
@@ -127,10 +128,18 @@ public function test_rendering_post_template_with_main_query_loop_already_starte
 		$content .= '<!-- /wp:post-template -->';
 		$content .= '<!-- /wp:query -->';
 
-		$expected  = '<ul class="alignwide wp-block-post-template is-layout-flow wp-block-post-template-is-layout-flow wp-block-query-is-layout-flow">';
-		$expected .= '<li class="wp-block-post post-' . self::$post->ID . ' post type-post status-publish format-standard hentry category-uncategorized">';
-		$expected .= '<h2 class="wp-block-post-title">' . self::$post->post_title . '</h2>';
-		$expected .= '</li>';
+		$expected = '<ul class="alignwide wp-block-post-template is-layout-flow wp-block-post-template-is-layout-flow wp-block-query-is-layout-flow">';
+
+		// Find all the posts of the 'post' post type.
+		$wp_query_posts = new WP_Query( array( 'post_type' => 'post' ) );
+
+		while ( $wp_query_posts->have_posts() ) {
+			$wp_query_posts->the_post();
+			$expected .= '<li class="wp-block-post post-' . get_the_ID() . ' post type-post status-publish format-standard hentry category-uncategorized">';
+			$expected .= '<h2 class="wp-block-post-title">' . get_the_title() . '</h2>';
+			$expected .= '</li>';
+		}
+
 		$expected .= '</ul>';
 
 		// Update the post's content to have a query block for the same query as the main query.
@@ -156,4 +165,55 @@ public function test_rendering_post_template_with_main_query_loop_already_starte
 
 		$this->assertSame( $expected, $output, 'Unexpected parsed post content' );
 	}
+
+	/**
+	 * Tests that the `core/post-template` block rewinds the default query when not in a single post of any post type.
+	 */
+	public function test_rendering_post_template_with_main_query_loop_not_single_post() {
+		global $wp_query, $wp_the_query;
+
+		// Query block with post template block.
+		$content  = '<!-- wp:query {"query":{"inherit":true}} -->';
+		$content .= '<!-- wp:post-template {"align":"wide"} -->';
+		$content .= '<!-- wp:post-title /-->';
+		$content .= '<!-- /wp:post-template -->';
+		$content .= '<!-- /wp:query -->';
+
+		$expected = '<ul class="alignwide wp-block-post-template is-layout-flow wp-block-post-template-is-layout-flow wp-block-query-is-layout-flow">';
+
+		// Find all the posts of the 'post' post type.
+		$wp_query_posts = new WP_Query( array( 'post_type' => 'post' ) );
+
+		while ( $wp_query_posts->have_posts() ) {
+			$wp_query_posts->the_post();
+			$expected .= '<li class="wp-block-post post-' . get_the_ID() . ' post type-post status-publish format-standard hentry category-uncategorized">';
+			$expected .= '<h2 class="wp-block-post-title">' . get_the_title() . '</h2>';
+			$expected .= '</li>';
+		}
+
+		$expected .= '</ul>';
+
+		// Update the post's content to have a query block for the same query as the main query.
+		wp_update_post(
+			array(
+				'ID'                    => self::$post->ID,
+				'post_content'          => $content,
+				'post_content_filtered' => $content,
+			)
+		);
+
+		// Set main query to all posts.
+		$wp_query     = new WP_Query( array( 'post_type' => 'post' ) );
+		$wp_the_query = $wp_query;
+
+		// Get post content within main query loop.
+		$output = '';
+		while ( $wp_query->have_posts() ) {
+			$wp_query->the_post();
+
+			$output = get_echo( 'the_content' );
+		}
+
+		$this->assertSame( $expected, $output, 'Unexpected parsed post content' );
+	}
 }