diff --git a/lib/block-supports/layout.php b/lib/block-supports/layout.php
index b26ed9df659c28..01ad8cae629451 100644
--- a/lib/block-supports/layout.php
+++ b/lib/block-supports/layout.php
@@ -39,9 +39,33 @@ function gutenberg_register_layout_support( $block_type ) {
  * @return string                                CSS style.
  */
 function gutenberg_get_layout_style( $selector, $layout, $has_block_gap_support = false, $gap_value = null, $should_skip_gap_serialization = false, $fallback_gap_value = '0.5em', $block_spacing = null ) {
+	gutenberg_set_layout_style( $selector, $layout, $has_block_gap_support, $gap_value, $should_skip_gap_serialization, $fallback_gap_value, $block_spacing );
+
+	// Use a unique store to avoid conflicts with other stores and implementations.
+	$store     = WP_Style_Engine_CSS_Rules_Store_Gutenberg::get_store( 'block-supports/layout/' . md5( $selector ) );
+	$processor = new WP_Style_Engine_Processor_Gutenberg( $store );
+	return $processor->get_css( true );
+}
+
+/**
+ * Adds the provided layout to the "block-supports/layout" Style-Engine store.
+ *
+ * @param string  $selector                      CSS selector.
+ * @param array   $layout                        Layout object. The one that is passed has already checked the existence of default block layout.
+ * @param boolean $has_block_gap_support         Whether the theme has support for the block gap.
+ * @param string  $gap_value                     The block gap value to apply.
+ * @param boolean $should_skip_gap_serialization Whether to skip applying the user-defined value set in the editor.
+ * @param string  $fallback_gap_value            The block gap value to apply.
+ * @param array   $block_spacing                 Custom spacing set on the block.
+ *
+ * @return bool Returns true if the layout style was successfully generated, otherwise false.
+ */
+function gutenberg_set_layout_style( $selector, $layout, $has_block_gap_support = false, $gap_value = null, $should_skip_gap_serialization = false, $fallback_gap_value = '0.5em', $block_spacing = null ) {
 	$layout_type = isset( $layout['type'] ) ? $layout['type'] : 'default';
 
-	$style = '';
+	// Get the block-supports Style-Engine Store.
+	$store = WP_Style_Engine_CSS_Rules_Store_Gutenberg::get_store( 'block-supports/layout' );
+
 	if ( 'default' === $layout_type ) {
 		$content_size = isset( $layout['contentSize'] ) ? $layout['contentSize'] : '';
 		$wide_size    = isset( $layout['wideSize'] ) ? $layout['wideSize'] : '';
@@ -55,14 +79,16 @@ function gutenberg_get_layout_style( $selector, $layout, $has_block_gap_support
 		$wide_max_width_value = wp_strip_all_tags( explode( ';', $wide_max_width_value )[0] );
 
 		if ( $content_size || $wide_size ) {
-			$style  = "$selector > :where(:not(.alignleft):not(.alignright):not(.alignfull)) {";
-			$style .= 'max-width: ' . esc_html( $all_max_width_value ) . ';';
-			$style .= 'margin-left: auto !important;';
-			$style .= 'margin-right: auto !important;';
-			$style .= '}';
+			$store->add_rule( "$selector > :where(:not(.alignleft):not(.alignright):not(.alignfull))" )->add_declarations(
+				array(
+					'max-width'    => $all_max_width_value,
+					'margin-left'  => 'auto !important',
+					'margin-right' => 'auto !important',
+				)
+			);
 
-			$style .= "$selector > .alignwide { max-width: " . esc_html( $wide_max_width_value ) . ';}';
-			$style .= "$selector .alignfull { max-width: none; }";
+			$store->add_rule( "$selector > .alignwide" )->add_declarations( array( 'max-width' => $wide_max_width_value ) );
+			$store->add_rule( "$selector .alignfull" )->add_declarations( array( 'max-width' => 'none' ) );
 
 			if ( isset( $block_spacing ) ) {
 				$block_spacing_values = gutenberg_style_engine_get_block_supports_styles(
@@ -75,11 +101,11 @@ function gutenberg_get_layout_style( $selector, $layout, $has_block_gap_support
 				// They're added separately because padding might only be set on one side.
 				if ( isset( $block_spacing_values['declarations']['padding-right'] ) ) {
 					$padding_right = $block_spacing_values['declarations']['padding-right'];
-					$style        .= "$selector > .alignfull { margin-right:calc($padding_right * -1); }";
+					$store->add_rule( "$selector > .alignfull" )->add_declarations( array( 'margin-right' => "calc($padding_right * -1)" ) );
 				}
 				if ( isset( $block_spacing_values['declarations']['padding-left'] ) ) {
 					$padding_left = $block_spacing_values['declarations']['padding-left'];
-					$style       .= "$selector > .alignfull { margin-left: calc($padding_left * -1); }";
+					$store->add_rule( "$selector > .alignfull" )->add_declarations( array( 'margin-left' => "calc($padding_left * -1)" ) );
 				}
 			}
 		}
@@ -89,8 +115,18 @@ function gutenberg_get_layout_style( $selector, $layout, $has_block_gap_support
 				$gap_value = isset( $gap_value['top'] ) ? $gap_value['top'] : null;
 			}
 			if ( $gap_value && ! $should_skip_gap_serialization ) {
-				$style .= "$selector > * { margin-block-start: 0; margin-block-end: 0; }";
-				$style .= "$selector > * + * { margin-block-start: $gap_value; margin-block-end: 0; }";
+				$store->add_rule( "$selector > *" )->add_declarations(
+					array(
+						'margin-block-start' => '0',
+						'margin-block-end'   => '0',
+					)
+				);
+				$store->add_rule( "$selector > * + *" )->add_declarations(
+					array(
+						'margin-block-start' => $gap_value,
+						'margin-block-end'   => '0',
+					)
+				);
 			}
 		}
 	} elseif ( 'flex' === $layout_type ) {
@@ -113,7 +149,7 @@ function gutenberg_get_layout_style( $selector, $layout, $has_block_gap_support
 		}
 
 		if ( ! empty( $layout['flexWrap'] ) && 'nowrap' === $layout['flexWrap'] ) {
-			$style .= "$selector { flex-wrap: nowrap; }";
+			$store->add_rule( $selector )->add_declarations( array( 'flex-wrap' => 'nowrap' ) );
 		}
 
 		if ( $has_block_gap_support ) {
@@ -123,9 +159,7 @@ function gutenberg_get_layout_style( $selector, $layout, $has_block_gap_support
 				$gap_value  = $gap_row === $gap_column ? $gap_row : $gap_row . ' ' . $gap_column;
 			}
 			if ( $gap_value && ! $should_skip_gap_serialization ) {
-				$style .= "$selector {";
-				$style .= "gap: $gap_value;";
-				$style .= '}';
+				$store->add_rule( $selector )->add_declarations( array( 'gap' => $gap_value ) );
 			}
 		}
 
@@ -136,29 +170,26 @@ function gutenberg_get_layout_style( $selector, $layout, $has_block_gap_support
 			 * by custom css.
 			 */
 			if ( ! empty( $layout['justifyContent'] ) && array_key_exists( $layout['justifyContent'], $justify_content_options ) ) {
-				$style .= "$selector {";
-				$style .= "justify-content: {$justify_content_options[ $layout['justifyContent'] ]};";
-				$style .= '}';
+				$store->add_rule( $selector )->add_declarations( array( 'justify-content' => $justify_content_options[ $layout['justifyContent'] ] ) );
 			}
 
 			if ( ! empty( $layout['verticalAlignment'] ) && array_key_exists( $layout['verticalAlignment'], $vertical_alignment_options ) ) {
-				$style .= "$selector {";
-				$style .= "align-items: {$vertical_alignment_options[ $layout['verticalAlignment'] ]};";
-				$style .= '}';
+				$store->add_rule( $selector )->add_declarations( array( 'align-items' => $vertical_alignment_options[ $layout['verticalAlignment'] ] ) );
 			}
 		} else {
-			$style .= "$selector {";
-			$style .= 'flex-direction: column;';
+			$store->add_rule( $selector )->add_declarations(
+				array(
+					'flex-direction' => 'column',
+					'align-items'    => 'flex-start',
+				)
+			);
 			if ( ! empty( $layout['justifyContent'] ) && array_key_exists( $layout['justifyContent'], $justify_content_options ) ) {
-				$style .= "align-items: {$justify_content_options[ $layout['justifyContent'] ]};";
-			} else {
-				$style .= 'align-items: flex-start;';
+				$store->add_rule( $selector )->add_declarations( array( 'align-items' => $justify_content_options[ $layout['justifyContent'] ] ) );
 			}
-			$style .= '}';
 		}
 	}
 
-	return $style;
+	return ! empty( $store->get_all_rules() );
 }
 
 /**
@@ -244,12 +275,12 @@ function gutenberg_render_layout_support_flag( $block_content, $block ) {
 	// If a block's block.json skips serialization for spacing or spacing.blockGap,
 	// don't apply the user-defined value to the styles.
 	$should_skip_gap_serialization = gutenberg_should_skip_block_supports_serialization( $block_type, 'spacing', 'blockGap' );
-	$style                         = gutenberg_get_layout_style( ".$block_classname.$container_class", $used_layout, $has_block_gap_support, $gap_value, $should_skip_gap_serialization, $fallback_gap_value, $block_spacing );
+	$has_style                     = gutenberg_set_layout_style( ".$block_classname.$container_class", $used_layout, $has_block_gap_support, $gap_value, $should_skip_gap_serialization, $fallback_gap_value, $block_spacing );
 
 	// Only add container class and enqueue block support styles if unique styles were generated.
-	if ( ! empty( $style ) ) {
+	if ( $has_style ) {
 		$class_names[] = $container_class;
-		wp_enqueue_block_support_styles( $style );
+		gutenberg_enqueue_style_engine_store( 'block-supports/layout' );
 	}
 
 	// This assumes the hook only applies to blocks with a single wrapper.
diff --git a/lib/compat/wordpress-6.1/script-loader.php b/lib/compat/wordpress-6.1/script-loader.php
index b3995178431e90..658bd0e3b349d6 100644
--- a/lib/compat/wordpress-6.1/script-loader.php
+++ b/lib/compat/wordpress-6.1/script-loader.php
@@ -23,10 +23,7 @@
  * @param int    $priority To set the priority for the add_action.
  */
 function gutenberg_enqueue_block_support_styles( $style, $priority = 10 ) {
-	$action_hook_name = 'wp_footer';
-	if ( wp_is_block_theme() ) {
-		$action_hook_name = 'wp_head';
-	}
+	$action_hook_name = wp_is_block_theme() ? 'wp_head' : 'wp_footer';
 	add_action(
 		$action_hook_name,
 		static function () use ( $style ) {
@@ -36,6 +33,27 @@ static function () use ( $style ) {
 	);
 }
 
+/**
+ * This function takes care of adding inline styles
+ * from a Style-Engine store.
+ *
+ * @param string $store_name The name of the store.
+ */
+function gutenberg_enqueue_style_engine_store( $store_name ) {
+	$action_hook_name = wp_is_block_theme() ? 'wp_head' : 'wp_footer';
+	add_action(
+		$action_hook_name,
+		static function () use ( $store_name ) {
+			$css = ( new WP_Style_Engine_Processor_Gutenberg(
+				WP_Style_Engine_CSS_Rules_Store_Gutenberg::get_store( $store_name )
+			) )->get_css( true );
+			if ( $css ) {
+				echo '<style id="wp-style-engine-' . esc_attr( str_replace( '/', '-', $store_name ) ) . '">' . $css . '</style>';
+			}
+		}
+	);
+}
+
 /**
  * This applies a filter to the list of style nodes that comes from `get_style_nodes` in WP_Theme_JSON.
  * This particular filter removes all of the blocks from the array.
diff --git a/packages/style-engine/class-wp-style-engine-processor.php b/packages/style-engine/class-wp-style-engine-processor.php
index 646ea43e7261a8..e23bda25f8b5c7 100644
--- a/packages/style-engine/class-wp-style-engine-processor.php
+++ b/packages/style-engine/class-wp-style-engine-processor.php
@@ -37,9 +37,11 @@ public function __construct( WP_Style_Engine_CSS_Rules_Store $store ) {
 	/**
 	 * Get the CSS rules as a string.
 	 *
+	 * @param bool $remove_printed_rules Whether to remove printed rules.
+	 *
 	 * @return string The computed CSS.
 	 */
-	public function get_css() {
+	public function get_css( $remove_printed_rules = false ) {
 		// Combine CSS selectors that have identical declarations.
 		$this->combine_rules_selectors();
 
@@ -47,7 +49,12 @@ public function get_css() {
 		$css   = '';
 		$rules = $this->store->get_all_rules();
 		foreach ( $rules as $rule ) {
+			// Add the CSS.
 			$css .= $rule->get_css();
+			if ( $remove_printed_rules ) {
+				// Remove the rule from the store to avoid double-rendering.
+				$this->store->remove_rule( $rule->get_selector() );
+			}
 		}
 		return $css;
 	}