diff --git a/src/wp-includes/default-filters.php b/src/wp-includes/default-filters.php
index a4ecf677e2af1..a4758c3c02374 100644
--- a/src/wp-includes/default-filters.php
+++ b/src/wp-includes/default-filters.php
@@ -606,7 +606,8 @@
 add_action( 'enqueue_block_assets', 'wp_enqueue_classic_theme_styles' );
 add_action( 'enqueue_block_assets', 'wp_enqueue_registered_block_scripts_and_styles' );
 add_action( 'enqueue_block_assets', 'enqueue_block_styles_assets', 30 );
-add_action( 'wp_default_styles', 'wp_load_classic_theme_block_styles_on_demand', 0 ); // Must happen before wp_default_styles() and register_core_block_style_handles().
+add_action( 'init', 'wp_load_classic_theme_block_styles_on_demand', 8 ); // Must happen before register_core_block_style_handles() at priority 9.
+add_action( 'wp_default_styles', 'wp_load_classic_theme_block_styles_on_demand', 0 ); // Must happen before wp_default_styles() when WP_Styles is constructed before init priority 9.
 /*
  * `wp_enqueue_registered_block_scripts_and_styles` is bound to both
  * `enqueue_block_editor_assets` and `enqueue_block_assets` hooks
diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 134d86c26a08a..3ce18d4429236 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -3677,7 +3677,10 @@ function wp_remove_surrounding_empty_script_tags( $contents ) {
  * the filters are added to cause {@see wp_should_load_separate_core_block_assets()} to return true.
  *
  * @since 6.9.0
- * @since 7.0.0 This is now invoked at the `wp_default_styles` action with priority 0 instead of at `init` with priority 8.
+ * @since 7.0.0 This is also invoked at the `wp_default_styles` action with priority 0 so that filters are present when
+ *              `WP_Styles` is constructed before `init` priority 9. The `init` action at priority 8 is retained so
+ *              `register_core_block_style_handles()` can opt in to separate block assets without having to construct
+ *              `WP_Styles` first.
  *
  * @see _add_default_theme_supports()
  */
@@ -3692,7 +3695,9 @@ function wp_load_classic_theme_block_styles_on_demand(): void {
 	 * `wp_template_enhancement_output_buffer` filters added, but do so at priority zero so that applications which
 	 * wish to stream responses can more easily turn this off.
 	 */
-	add_filter( 'wp_should_output_buffer_template_for_enhancement', '__return_true', 0 );
+	if ( false === has_filter( 'wp_should_output_buffer_template_for_enhancement', '__return_true' ) ) {
+		add_filter( 'wp_should_output_buffer_template_for_enhancement', '__return_true', 0 );
+	}
 
 	// If a site has opted out of the template enhancement output buffer, then bail.
 	if ( ! wp_should_output_buffer_template_for_enhancement() ) {
@@ -3707,7 +3712,9 @@ function wp_load_classic_theme_block_styles_on_demand(): void {
 	 * this to be easily overridden by themes which wish to opt out. If a site has explicitly opted out of loading
 	 * separate block styles, then abort.
 	 */
-	add_filter( 'should_load_separate_core_block_assets', '__return_true', 0 );
+	if ( false === has_filter( 'should_load_separate_core_block_assets', '__return_true' ) ) {
+		add_filter( 'should_load_separate_core_block_assets', '__return_true', 0 );
+	}
 	if ( ! wp_should_load_separate_core_block_assets() ) {
 		return;
 	}
@@ -3717,13 +3724,17 @@ function wp_load_classic_theme_block_styles_on_demand(): void {
 	 * As above, a priority of zero allows for this to be easily overridden by themes which wish to opt out. If a site
 	 * has explicitly opted out of loading block styles on demand, then abort.
 	 */
-	add_filter( 'should_load_block_assets_on_demand', '__return_true', 0 );
+	if ( false === has_filter( 'should_load_block_assets_on_demand', '__return_true' ) ) {
+		add_filter( 'should_load_block_assets_on_demand', '__return_true', 0 );
+	}
 	if ( ! wp_should_load_block_assets_on_demand() ) {
 		return;
 	}
 
 	// Add hooks which require the presence of the output buffer. Ideally the above two filters could be added here, but they run too early.
-	add_action( 'wp_template_enhancement_output_buffer_started', 'wp_hoist_late_printed_styles' );
+	if ( false === has_action( 'wp_template_enhancement_output_buffer_started', 'wp_hoist_late_printed_styles' ) ) {
+		add_action( 'wp_template_enhancement_output_buffer_started', 'wp_hoist_late_printed_styles' );
+	}
 }
 
 /**
diff --git a/tests/phpunit/tests/blocks/classicThemeBlockStylesOnDemand.php b/tests/phpunit/tests/blocks/classicThemeBlockStylesOnDemand.php
new file mode 100644
index 0000000000000..ceaa1c35097cf
--- /dev/null
+++ b/tests/phpunit/tests/blocks/classicThemeBlockStylesOnDemand.php
@@ -0,0 +1,128 @@
+<?php
+
+/**
+ * Tests loading block opinionated (theme) styles on demand in classic themes.
+ *
+ * @package WordPress
+ * @subpackage Blocks
+ *
+ * @group blocks
+ */
+class Tests_Blocks_ClassicThemeBlockStylesOnDemand extends WP_UnitTestCase {
+
+	/**
+	 * @var WP_Styles|null
+	 */
+	protected $original_wp_styles;
+
+	public function set_up() {
+		parent::set_up();
+
+		global $wp_styles;
+		$this->original_wp_styles = $wp_styles;
+	}
+
+	public function tear_down() {
+		global $wp_styles;
+		$wp_styles = $this->original_wp_styles;
+
+		parent::tear_down();
+	}
+
+	/**
+	 * @ticket 65272
+	 *
+	 * @covers ::wp_load_classic_theme_block_styles_on_demand
+	 * @covers ::register_core_block_style_handles
+	 */
+	public function test_register_core_block_style_handles_without_prior_wp_styles() {
+		global $wp_styles;
+		$wp_styles = null;
+
+		remove_all_filters( 'should_load_separate_core_block_assets' );
+		remove_all_filters( 'should_load_block_assets_on_demand' );
+		remove_all_filters( 'wp_should_output_buffer_template_for_enhancement' );
+
+		remove_all_actions( 'init' );
+		remove_all_actions( 'wp_default_styles' );
+
+		add_action( 'init', 'wp_load_classic_theme_block_styles_on_demand', 8 );
+		add_action( 'init', 'register_core_block_style_handles', 9 );
+		add_action( 'wp_default_styles', 'wp_load_classic_theme_block_styles_on_demand', 0 );
+		add_action( 'wp_default_styles', 'wp_default_styles' );
+
+		add_theme_support( 'wp-block-styles' );
+
+		$this->assertFalse( $wp_styles instanceof WP_Styles, 'Expected WP_Styles to not be constructed yet.' );
+		$this->assertFalse( wp_should_load_separate_core_block_assets(), 'Expected separate core block assets to be disabled before init.' );
+
+		do_action( 'init' );
+
+		$this->assertTrue( wp_should_load_separate_core_block_assets(), 'Expected separate core block assets to be enabled after init.' );
+		$this->assertTrue( wp_style_is( 'wp-block-quote-theme', 'registered' ), 'Expected the Quote block theme stylesheet to be registered.' );
+	}
+
+	/**
+	 * @ticket 65272
+	 *
+	 * @covers ::wp_load_classic_theme_block_styles_on_demand
+	 */
+	public function test_wp_load_classic_theme_block_styles_on_demand_does_not_duplicate_hooks() {
+		switch_theme( 'default' );
+
+		remove_all_filters( 'should_load_separate_core_block_assets' );
+		remove_all_filters( 'should_load_block_assets_on_demand' );
+		remove_all_filters( 'wp_should_output_buffer_template_for_enhancement' );
+		remove_all_actions( 'wp_template_enhancement_output_buffer_started' );
+
+		wp_load_classic_theme_block_styles_on_demand();
+		wp_load_classic_theme_block_styles_on_demand();
+
+		global $wp_filter;
+
+		$this->assertSame( 0, has_filter( 'should_load_separate_core_block_assets', '__return_true' ) );
+		$this->assertCount( 1, $wp_filter['should_load_separate_core_block_assets']->callbacks[0] );
+		$this->assertCount( 1, $wp_filter['should_load_block_assets_on_demand']->callbacks[0] );
+		$this->assertCount( 1, $wp_filter['wp_should_output_buffer_template_for_enhancement']->callbacks[0] );
+		$this->assertCount( 1, $wp_filter['wp_template_enhancement_output_buffer_started']->callbacks[10] );
+	}
+
+	/**
+	 * @ticket 64846
+	 * @ticket 65272
+	 *
+	 * @covers ::wp_load_classic_theme_block_styles_on_demand
+	 * @covers ::wp_default_styles
+	 */
+	public function test_wp_block_library_uses_common_css_when_wp_styles_constructed_before_init() {
+		global $wp_styles;
+		$wp_styles = null;
+
+		remove_all_filters( 'should_load_separate_core_block_assets' );
+		remove_all_filters( 'should_load_block_assets_on_demand' );
+		remove_all_filters( 'wp_should_output_buffer_template_for_enhancement' );
+
+		remove_all_actions( 'init' );
+		remove_all_actions( 'wp_default_styles' );
+
+		add_action( 'init', 'wp_load_classic_theme_block_styles_on_demand', 8 );
+		add_action( 'init', 'register_core_block_style_handles', 9 );
+		add_action( 'wp_default_styles', 'wp_load_classic_theme_block_styles_on_demand', 0 );
+		add_action( 'wp_default_styles', 'wp_default_styles' );
+
+		add_theme_support( 'wp-block-styles' );
+
+		wp_styles();
+
+		$this->assertSame(
+			'/' . WPINC . '/css/dist/block-library/common.css',
+			wp_styles()->registered['wp-block-library']->src,
+			'Expected wp-block-library to use common.css when separate core block assets are enabled.'
+		);
+
+		do_action( 'init' );
+
+		$this->assertTrue( wp_should_load_separate_core_block_assets(), 'Expected separate core block assets to remain enabled after init.' );
+		$this->assertTrue( wp_style_is( 'wp-block-quote-theme', 'registered' ), 'Expected the Quote block theme stylesheet to be registered after init.' );
+	}
+}