diff --git a/src/wp-includes/block-supports/block-visibility.php b/src/wp-includes/block-supports/block-visibility.php
index 1ba208e30c92e..9ee726ee18a69 100644
--- a/src/wp-includes/block-supports/block-visibility.php
+++ b/src/wp-includes/block-supports/block-visibility.php
@@ -20,16 +20,24 @@
 function wp_render_block_visibility_support( $block_content, $block ) {
 	$block_type = WP_Block_Type_Registry::get_instance()->get_registered( $block['blockName'] );
 
-	if ( ! $block_type || ! block_has_support( $block_type, 'visibility', true ) ) {
+	if ( ! $block_type ) {
 		return $block_content;
 	}
 
 	$block_visibility = $block['attrs']['metadata']['blockVisibility'] ?? null;
 
+	// Hide the block whenever the value is boolean false, regardless of the
+	// block's current visibility support. This prevents blocks that previously
+	// supported visibility from unintentionally appearing on the front end
+	// after their support was disabled.
 	if ( false === $block_visibility ) {
 		return '';
 	}
 
+	if ( ! block_has_support( $block_type, 'visibility', true ) ) {
+		return $block_content;
+	}
+
 	if ( is_array( $block_visibility ) && ! empty( $block_visibility ) ) {
 		$viewport_config = $block_visibility['viewport'] ?? null;
 
diff --git a/tests/phpunit/tests/block-supports/block-visibility.php b/tests/phpunit/tests/block-supports/block-visibility.php
index 4f24b931744f8..f5299b32251b2 100644
--- a/tests/phpunit/tests/block-supports/block-visibility.php
+++ b/tests/phpunit/tests/block-supports/block-visibility.php
@@ -80,12 +80,13 @@ public function test_block_visibility_support_hides_block_when_visibility_false(
 	}
 
 	/**
-	 * Tests that block visibility support renders block normally when visibility is false
-	 * but blockVisibility support is not opted in.
+	 * Tests that block visibility support hides the block when visibility is false
+	 * even when blockVisibility support is not opted in.
 	 *
 	 * @ticket 64061
+	 * @ticket 65389
 	 */
-	public function test_block_visibility_support_shows_block_when_support_not_opted_in(): void {
+	public function test_block_visibility_support_hides_block_when_visibility_false_even_without_support(): void {
 		$this->register_visibility_block_with_support(
 			'test/visibility-block',
 			array( 'visibility' => false )
@@ -103,7 +104,7 @@ public function test_block_visibility_support_shows_block_when_support_not_opted
 
 		$result = wp_render_block_visibility_support( $block_content, $block );
 
-		$this->assertSame( $block_content, $result, 'Block content should remain unchanged when blockVisibility support is not opted in.' );
+		$this->assertSame( '', $result, 'Block content should be empty when blockVisibility is false, even without visibility support.' );
 	}
 
 	/**