diff --git a/lib/blocks.php b/lib/blocks.php
index a8083466a04053..0b11041d0576de 100644
--- a/lib/blocks.php
+++ b/lib/blocks.php
@@ -174,6 +174,13 @@ function gutenberg_render_block( $block ) {
 	 * @return string          Updated post content.
 	 */
 	function do_blocks( $content ) {
+		// If there are blocks in this content, we shouldn't run wpautop() on it later.
+		$priority = has_filter( 'the_content', 'wpautop' );
+		if ( false !== $priority && doing_filter( 'the_content' ) && has_blocks( $content ) ) {
+			remove_filter( 'the_content', 'wpautop', $priority );
+			add_filter( 'the_content', '_restore_wpautop_hook', $priority + 1 );
+		}
+
 		$blocks = gutenberg_parse_blocks( $content );
 		$output = '';
 
@@ -187,6 +194,28 @@ function do_blocks( $content ) {
 	add_filter( 'the_content', 'do_blocks', 7 ); // BEFORE do_shortcode() and oembed.
 }
 
+if ( ! function_exists( '_restore_wpautop_hook' ) ) {
+	/**
+	 * If do_blocks() needs to remove wpautop() from the `the_content` filter,
+	 * this re-adds it afterwards, for subsequent `the_content` usage.
+	 *
+	 * @access private
+	 *
+	 * @since 4.6.0
+	 *
+	 * @param string $content The post content running through this filter.
+	 * @return string The unmodified content.
+	 */
+	function _restore_wpautop_hook( $content ) {
+		$current_priority = has_filter( 'the_content', '_restore_wpautop_hook' );
+
+		add_filter( 'the_content', 'wpautop', $current_priority - 1 );
+		remove_filter( 'the_content', '_restore_wpautop_hook', $current_priority );
+
+		return $content;
+	}
+}
+
 if ( ! function_exists( 'strip_dynamic_blocks' ) ) {
 	/**
 	 * Remove all dynamic blocks from the given content.
diff --git a/lib/compat.php b/lib/compat.php
index 88b417491a89e9..03af8d9302af14 100644
--- a/lib/compat.php
+++ b/lib/compat.php
@@ -99,23 +99,6 @@ function gutenberg_add_rest_nonce_to_heartbeat_response_headers( $response ) {
 }
 add_filter( 'wp_refresh_nonces', 'gutenberg_add_rest_nonce_to_heartbeat_response_headers' );
 
-/**
- * As a substitute for the default content `wpautop` filter, applies autop
- * behavior only for posts where content does not contain blocks.
- *
- * @param  string $content Post content.
- * @return string          Paragraph-converted text if non-block content.
- */
-function gutenberg_wpautop( $content ) {
-	if ( has_blocks( $content ) ) {
-		return $content;
-	}
-
-	return wpautop( $content );
-}
-remove_filter( 'the_content', 'wpautop' );
-add_filter( 'the_content', 'gutenberg_wpautop', 6 );
-
 /**
  * Check if we need to load the block warning in the Classic Editor.
  *