diff --git a/src/wp-includes/class-wp-customize-manager.php b/src/wp-includes/class-wp-customize-manager.php
index c2198acf20f66..bddabfab01a40 100644
--- a/src/wp-includes/class-wp-customize-manager.php
+++ b/src/wp-includes/class-wp-customize-manager.php
@@ -5410,7 +5410,7 @@ public function register_controls() {
 				$this,
 				'header_image',
 				array(
-					'default'        => sprintf( get_theme_support( 'custom-header', 'default-image' ), get_template_directory_uri(), get_stylesheet_directory_uri() ),
+					'default'        => current_theme_supports( 'custom-header', 'random-default' ) ? 'random-default-image' : sprintf( get_theme_support( 'custom-header', 'default-image' ), get_template_directory_uri(), get_stylesheet_directory_uri() ),
 					'theme_supports' => 'custom-header',
 				)
 			)
diff --git a/tests/phpunit/tests/customize/manager.php b/tests/phpunit/tests/customize/manager.php
index bedf0b39b3e95..9c92a199288ca 100644
--- a/tests/phpunit/tests/customize/manager.php
+++ b/tests/phpunit/tests/customize/manager.php
@@ -3683,6 +3683,49 @@ public function test_sanitize_external_header_video_trim() {
 			$this->assertSame( $video_url, $sanitized );
 		}
 	}
+
+	/**
+	 * @ticket 46128
+	 *
+	 * @dataProvider data_header_image_setting_default
+	 *
+	 * @param bool   $random_default   Whether to randomize default headers.
+	 * @param string $expected_default Expected setting default.
+	 */
+	public function test_header_image_setting_default( $random_default, $expected_default ) {
+		global $_wp_theme_features;
+
+		$custom_header_support = isset( $_wp_theme_features['custom-header'] ) ? $_wp_theme_features['custom-header'] : null;
+
+		try {
+			$_wp_theme_features['custom-header'][0] = array(
+				'default-image'  => 'https://example.org/header.jpg',
+				'random-default' => $random_default,
+			);
+
+			$this->manager->register_controls();
+
+			$this->assertSame( $expected_default, $this->manager->get_setting( 'header_image' )->default );
+		} finally {
+			if ( null === $custom_header_support ) {
+				unset( $_wp_theme_features['custom-header'] );
+			} else {
+				$_wp_theme_features['custom-header'] = $custom_header_support;
+			}
+		}
+	}
+
+	/**
+	 * Data provider for test_header_image_setting_default().
+	 *
+	 * @return array[] Test parameters.
+	 */
+	public function data_header_image_setting_default() {
+		return array(
+			'random default headers' => array( true, 'random-default-image' ),
+			'fixed default header'   => array( false, 'https://example.org/header.jpg' ),
+		);
+	}
 }
 
 require_once ABSPATH . WPINC . '/class-wp-customize-setting.php';