diff --git a/src/wp-includes/block-template.php b/src/wp-includes/block-template.php
index df3735b238e4f..7b09c3fe77d10 100644
--- a/src/wp-includes/block-template.php
+++ b/src/wp-includes/block-template.php
@@ -301,7 +301,78 @@ function get_the_block_template_html() {
 
 	// Wrap block template in .wp-site-blocks to allow for specific descendant styles
 	// (e.g. `.wp-site-blocks > *`).
-	return '<div class="wp-site-blocks">' . $content . '</div>';
+	$template_html = '<div class="wp-site-blocks">' . $content . '</div>';
+
+	return _block_template_skip_link_markup( $template_html );
+}
+
+/**
+ * Inserts the block template skip link into the template HTML.
+ *
+ * Uses the HTML API to ensure that the main content element has an ID and to
+ * inject the skip-link anchor before the block template wrapper.
+ *
+ * @access private
+ * @since 7.0.0
+ *
+ * @param string $template_html Block template markup.
+ * @return string Modified markup with skip link when applicable.
+ */
+function _block_template_skip_link_markup( string $template_html ): string {
+
+	// Back-compat for plugins that disable functionality by unhooking this action.
+	if ( ! has_action( 'wp_footer', 'the_block_template_skip_link' ) ) {
+		return $template_html;
+	}
+
+	// Ensure a skip-link target exists and has an ID.
+	$processor           = new WP_HTML_Tag_Processor( $template_html );
+	$skip_link_target_id = null;
+
+	// Get the first <main> element.
+	if ( $processor->next_tag( 'MAIN' ) ) {
+		$skip_link_target_id = $processor->get_attribute( 'id' );
+		if ( ! is_string( $skip_link_target_id ) || '' === trim( $skip_link_target_id ) ) {
+			$skip_link_target_id = 'wp--skip-link--target';
+			$processor->set_attribute( 'id', $skip_link_target_id );
+		}
+	}
+
+	// Early exit if a skip-link target can't be located.
+	if ( null === $skip_link_target_id ) {
+		return $template_html;
+	}
+
+	// Apply any updates from setting the main ID.
+	$template_html = $processor->get_updated_html();
+
+	// Anonymous subclass of WP_HTML_Tag_Processor to access protected bookmark spans.
+	$inserter = new class( $template_html ) extends WP_HTML_Tag_Processor {
+		/**
+		 * Inserts text before the current token.
+		 *
+		 * @param string $text Text to insert.
+		 */
+		public function insert_before( string $text ) {
+			$this->set_bookmark( 'here' );
+			$this->lexical_updates[] = new WP_HTML_Text_Replacement( $this->bookmarks['here']->start, 0, $text );
+		}
+	};
+
+	while ( $inserter->next_tag() ) {
+		if ( 'DIV' === $inserter->get_tag() && $inserter->has_class( 'wp-site-blocks' ) ) {
+			$skip_link = sprintf(
+				'<a class="skip-link screen-reader-text" id="wp-skip-link" href="%s">%s</a>',
+				esc_url( '#' . $skip_link_target_id ),
+				/* translators: Hidden accessibility text. */
+				esc_html__( 'Skip to content' )
+			);
+			$inserter->insert_before( $skip_link );
+			break;
+		}
+	}
+
+	return $inserter->get_updated_html();
 }
 
 /**
diff --git a/src/wp-includes/css/wp-block-template-skip-link.css b/src/wp-includes/css/wp-block-template-skip-link.css
new file mode 100644
index 0000000000000..4176599ad0667
--- /dev/null
+++ b/src/wp-includes/css/wp-block-template-skip-link.css
@@ -0,0 +1,27 @@
+.skip-link.screen-reader-text {
+	border: 0;
+	clip-path: inset(50%);
+	height: 1px;
+	margin: -1px;
+	overflow: hidden;
+	padding: 0;
+	position: absolute !important;
+	width: 1px;
+	word-wrap: normal !important;
+}
+
+.skip-link.screen-reader-text:focus {
+	background-color: #eee;
+	clip-path: none;
+	color: #444;
+	display: block;
+	font-size: 1em;
+	height: auto;
+	left: 5px;
+	line-height: normal;
+	padding: 15px 23px 14px;
+	text-decoration: none;
+	top: 5px;
+	width: auto;
+	z-index: 100000;
+}
diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 89ef4acf734f3..326248122f129 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -1605,6 +1605,9 @@ function wp_default_styles( $styles ) {
 	$styles->add( 'wp-pointer', "/wp-includes/css/wp-pointer$suffix.css", array( 'dashicons' ) );
 	$styles->add( 'customize-preview', "/wp-includes/css/customize-preview$suffix.css", array( 'dashicons' ) );
 	$styles->add( 'wp-empty-template-alert', "/wp-includes/css/wp-empty-template-alert$suffix.css" );
+	$skip_link_style_path = WPINC . "/css/wp-block-template-skip-link$suffix.css";
+	$styles->add( 'wp-block-template-skip-link', $skip_link_style_path );
+	$styles->add_data( 'wp-block-template-skip-link', 'path', ABSPATH . $skip_link_style_path );
 
 	// External libraries and friends.
 	$styles->add( 'imgareaselect', '/wp-includes/js/imgareaselect/imgareaselect.css', array(), '0.9.8' );
diff --git a/src/wp-includes/theme-templates.php b/src/wp-includes/theme-templates.php
index eed0fb9b2b029..cc3af0d53d8f5 100644
--- a/src/wp-includes/theme-templates.php
+++ b/src/wp-includes/theme-templates.php
@@ -99,10 +99,11 @@ function wp_filter_wp_template_unique_post_slug( $override_slug, $slug, $post_id
 }
 
 /**
- * Enqueues the skip-link script & styles.
+ * Enqueues the skip-link styles.
  *
  * @access private
  * @since 6.4.0
+ * @since 7.0.0 A script is no longer printed in favor of being added via {@see _block_template_skip_link_markup()}.
  *
  * @global string $_wp_current_template_content
  */
@@ -125,96 +126,7 @@ function wp_enqueue_block_template_skip_link() {
 		return;
 	}
 
-	$skip_link_styles = '
-		.skip-link.screen-reader-text {
-			border: 0;
-			clip-path: inset(50%);
-			height: 1px;
-			margin: -1px;
-			overflow: hidden;
-			padding: 0;
-			position: absolute !important;
-			width: 1px;
-			word-wrap: normal !important;
-		}
-
-		.skip-link.screen-reader-text:focus {
-			background-color: #eee;
-			clip-path: none;
-			color: #444;
-			display: block;
-			font-size: 1em;
-			height: auto;
-			left: 5px;
-			line-height: normal;
-			padding: 15px 23px 14px;
-			text-decoration: none;
-			top: 5px;
-			width: auto;
-			z-index: 100000;
-		}';
-
-	$handle = 'wp-block-template-skip-link';
-
-	/**
-	 * Print the skip-link styles.
-	 */
-	wp_register_style( $handle, false );
-	wp_add_inline_style( $handle, $skip_link_styles );
-	wp_enqueue_style( $handle );
-
-	/**
-	 * Enqueue the skip-link script.
-	 */
-	ob_start();
-	?>
-	<script>
-	( function() {
-		var skipLinkTarget = document.querySelector( 'main' ),
-			sibling,
-			skipLinkTargetID,
-			skipLink;
-
-		// Early exit if a skip-link target can't be located.
-		if ( ! skipLinkTarget ) {
-			return;
-		}
-
-		/*
-		 * Get the site wrapper.
-		 * The skip-link will be injected in the beginning of it.
-		 */
-		sibling = document.querySelector( '.wp-site-blocks' );
-
-		// Early exit if the root element was not found.
-		if ( ! sibling ) {
-			return;
-		}
-
-		// Get the skip-link target's ID, and generate one if it doesn't exist.
-		skipLinkTargetID = skipLinkTarget.id;
-		if ( ! skipLinkTargetID ) {
-			skipLinkTargetID = 'wp--skip-link--target';
-			skipLinkTarget.id = skipLinkTargetID;
-		}
-
-		// Create the skip link.
-		skipLink = document.createElement( 'a' );
-		skipLink.classList.add( 'skip-link', 'screen-reader-text' );
-		skipLink.id = 'wp-skip-link';
-		skipLink.href = '#' + skipLinkTargetID;
-		skipLink.innerText = '<?php /* translators: Hidden accessibility text. Do not use HTML entities (&nbsp;, etc.). */ esc_html_e( 'Skip to content' ); ?>';
-
-		// Inject the skip link.
-		sibling.parentElement.insertBefore( skipLink, sibling );
-	}() );
-	</script>
-	<?php
-	$skip_link_script = wp_remove_surrounding_empty_script_tags( ob_get_clean() );
-	$script_handle    = 'wp-block-template-skip-link';
-	wp_register_script( $script_handle, false, array(), false, array( 'in_footer' => true ) );
-	wp_add_inline_script( $script_handle, $skip_link_script );
-	wp_enqueue_script( $script_handle );
+	wp_enqueue_style( 'wp-block-template-skip-link' );
 }
 
 /**
diff --git a/tests/phpunit/tests/block-template-utils.php b/tests/phpunit/tests/block-template-utils.php
index e5255ba5ae011..f46f044a04327 100644
--- a/tests/phpunit/tests/block-template-utils.php
+++ b/tests/phpunit/tests/block-template-utils.php
@@ -297,6 +297,76 @@ public function data_remove_theme_attribute_in_block_template_content() {
 		);
 	}
 
+	/**
+	 * Tests adding the skip link (or not).
+	 *
+	 * @ticket 64361
+	 *
+	 * @covers ::_block_template_skip_link_markup
+	 *
+	 * @dataProvider data_provider_to_test_block_template_skip_link_markup
+	 */
+	public function test_block_template_skip_link_markup( ?Closure $set_up, string $template_html, string $expected ) {
+		if ( $set_up instanceof Closure ) {
+			$set_up();
+		}
+		$this->assertEqualHTML( $expected, _block_template_skip_link_markup( $template_html ) );
+	}
+
+	/**
+	 * Data provider for test_block_template_skip_link_markup.
+	 *
+	 * @return array<string, array<string, mixed>>
+	 */
+	public function data_provider_to_test_block_template_skip_link_markup(): array {
+		return array(
+			'inserts_link_and_adds_main_id_when_missing' => array(
+				'set_up'        => null,
+				'template_html' => '<div class="wp-site-blocks"><main>Content</main></div>',
+				'expected'      => '
+					<a class="skip-link screen-reader-text" id="wp-skip-link" href="#wp--skip-link--target">Skip to content</a>
+					<div class="wp-site-blocks"><main id="wp--skip-link--target">Content</main></div>
+				',
+			),
+			'uses_existing_main_id'                      => array(
+				'set_up'        => null,
+				'template_html' => '<div class="wp-site-blocks"><main id="custom-id">Content</main></div>',
+				'expected'      => '
+					<a class="skip-link screen-reader-text" id="wp-skip-link" href="#custom-id">Skip to content</a>
+					<div class="wp-site-blocks"><main id="custom-id">Content</main></div>
+				',
+			),
+			'main_has_boolean_id'                        => array(
+				'set_up'        => null,
+				'template_html' => '<div class="wp-site-blocks"><main id>Content</main></div>',
+				'expected'      => '
+					<a class="skip-link screen-reader-text" id="wp-skip-link" href="#wp--skip-link--target">Skip to content</a>
+					<div class="wp-site-blocks"><main id="wp--skip-link--target">Content</main></div>
+				',
+			),
+			'main_has_whitespace_id'                     => array(
+				'set_up'        => null,
+				'template_html' => '<div class="wp-site-blocks"><main id="   ">Content</main></div>',
+				'expected'      => '
+					<a class="skip-link screen-reader-text" id="wp-skip-link" href="#wp--skip-link--target">Skip to content</a>
+					<div class="wp-site-blocks"><main id="wp--skip-link--target">Content</main></div>
+				',
+			),
+			'action_removed'                             => array(
+				'set_up'        => static function () {
+					remove_action( 'wp_footer', 'the_block_template_skip_link' );
+				},
+				'template_html' => '<div class="wp-site-blocks"><main>Content</main></div>',
+				'expected'      => '<div class="wp-site-blocks"><main>Content</main></div>',
+			),
+			'main_missing'                               => array(
+				'set_up'        => null,
+				'template_html' => '<div class="wp-site-blocks"><div>Content</div></div>',
+				'expected'      => '<div class="wp-site-blocks"><div>Content</div></div>',
+			),
+		);
+	}
+
 	/**
 	 * Should retrieve the template from the theme files.
 	 */