diff --git a/packages/block-library/src/search/block.json b/packages/block-library/src/search/block.json
index b96f14f53c778c..54bb6b43635bdd 100644
--- a/packages/block-library/src/search/block.json
+++ b/packages/block-library/src/search/block.json
@@ -42,6 +42,7 @@
 	"supports": {
 		"align": [ "left", "center", "right" ],
 		"__experimentalBorder": {
+			"color": true,
 			"radius": true,
 			"__experimentalSkipSerialization": true
 		},
diff --git a/packages/block-library/src/search/edit.js b/packages/block-library/src/search/edit.js
index e279fcb0ad002b..7bb783ee0fd97f 100644
--- a/packages/block-library/src/search/edit.js
+++ b/packages/block-library/src/search/edit.js
@@ -72,6 +72,7 @@ export default function SearchEdit( {
 	} = attributes;
 
 	const borderRadius = style?.border?.radius;
+	const borderColor = style?.border?.color;
 	const borderProps = useBorderProps( attributes );
 
 	// Check for old deprecated numerical border radius. Done as a separate
@@ -83,6 +84,10 @@ export default function SearchEdit( {
 
 	const unitControlInstanceId = useInstanceId( UnitControl );
 	const unitControlInputId = `wp-block-search__width-${ unitControlInstanceId }`;
+	const isButtonPositionInside = 'button-inside' === buttonPosition;
+	const isButtonPositionOutside = 'button-outside' === buttonPosition;
+	const hasNoButton = 'no-button' === buttonPosition;
+	const hasOnlyButton = 'button-only' === buttonPosition;
 
 	const units = useCustomUnits( {
 		availableUnits: [ '%', 'px' ],
@@ -92,22 +97,19 @@ export default function SearchEdit( {
 	const getBlockClassNames = () => {
 		return classnames(
 			className,
-			'button-inside' === buttonPosition
+			! isButtonPositionInside ? borderProps.className : undefined,
+			isButtonPositionInside
 				? 'wp-block-search__button-inside'
 				: undefined,
-			'button-outside' === buttonPosition
+			isButtonPositionOutside
 				? 'wp-block-search__button-outside'
 				: undefined,
-			'no-button' === buttonPosition
-				? 'wp-block-search__no-button'
-				: undefined,
-			'button-only' === buttonPosition
-				? 'wp-block-search__button-only'
-				: undefined,
-			! buttonUseIcon && 'no-button' !== buttonPosition
+			hasNoButton ? 'wp-block-search__no-button' : undefined,
+			hasOnlyButton ? 'wp-block-search__button-only' : undefined,
+			! buttonUseIcon && ! hasNoButton
 				? 'wp-block-search__text-button'
 				: undefined,
-			buttonUseIcon && 'no-button' !== buttonPosition
+			buttonUseIcon && ! hasNoButton
 				? 'wp-block-search__icon-button'
 				: undefined
 		);
@@ -163,21 +165,30 @@ export default function SearchEdit( {
 	};
 
 	const getResizableSides = () => {
-		if ( 'button-only' === buttonPosition ) {
+		if ( hasOnlyButton ) {
 			return {};
 		}
 
 		return {
-			right: align === 'right' ? false : true,
-			left: align === 'right' ? true : false,
+			right: align !== 'right',
+			left: align === 'right',
 		};
 	};
 
 	const renderTextField = () => {
+		// If the input is inside the wrapper, the wrapper gets the border color styles/classes, not the input control.
+		const textFieldClasses = classnames(
+			'wp-block-search__input',
+			isButtonPositionInside ? undefined : borderProps.className
+		);
+		const textFieldStyles = isButtonPositionInside
+			? { borderRadius }
+			: borderProps.style;
+
 		return (
 			<input
-				className="wp-block-search__input"
-				style={ borderProps.style }
+				className={ textFieldClasses }
+				style={ textFieldStyles }
 				aria-label={ __( 'Optional placeholder text' ) }
 				// We hide the placeholder field's placeholder when there is a value. This
 				// stops screen readers from reading the placeholder field's placeholder
@@ -194,20 +205,29 @@ export default function SearchEdit( {
 	};
 
 	const renderButton = () => {
+		// If the button is inside the wrapper, the wrapper gets the border color styles/classes, not the button.
+		const buttonClasses = classnames(
+			'wp-block-search__button',
+			isButtonPositionInside ? undefined : borderProps.className
+		);
+		const buttonStyles = isButtonPositionInside
+			? { borderRadius }
+			: borderProps.style;
+
 		return (
 			<>
 				{ buttonUseIcon && (
 					<Button
 						icon={ search }
-						className="wp-block-search__button"
-						style={ borderProps.style }
+						className={ buttonClasses }
+						style={ buttonStyles }
 					/>
 				) }
 
 				{ ! buttonUseIcon && (
 					<RichText
-						className="wp-block-search__button"
-						style={ borderProps.style }
+						className={ buttonClasses }
+						style={ buttonStyles }
 						aria-label={ __( 'Button text' ) }
 						placeholder={ __( 'Add button text…' ) }
 						withoutInteractiveFormatting
@@ -240,7 +260,7 @@ export default function SearchEdit( {
 						label={ __( 'Change button position' ) }
 						controls={ buttonPositionControls }
 					/>
-					{ 'no-button' !== buttonPosition && (
+					{ ! hasNoButton && (
 						<ToolbarButton
 							title={ __( 'Use button with icon' ) }
 							icon={ buttonWithIcon }
@@ -329,13 +349,18 @@ export default function SearchEdit( {
 		radius ? `calc(${ radius } + ${ DEFAULT_INNER_PADDING })` : undefined;
 
 	const getWrapperStyles = () => {
+		const styles = {
+			borderColor,
+		};
+
 		const isNonZeroBorderRadius = parseInt( borderRadius, 10 ) !== 0;
 
-		if ( 'button-inside' === buttonPosition && isNonZeroBorderRadius ) {
+		if ( isButtonPositionInside && isNonZeroBorderRadius ) {
 			// We have button inside wrapper and a border radius value to apply.
 			// Add default padding so we don't get "fat" corners.
 			//
-			// CSS calc() is used here to support non-pixel units.
+			// CSS calc() is used here to support non-pixel units. The inline
+			// style using calc() will only apply if both values have units.
 
 			if ( typeof borderRadius === 'object' ) {
 				// Individual corner border radii present.
@@ -351,6 +376,7 @@ export default function SearchEdit( {
 					borderTopRightRadius: padBorderRadius( topRight ),
 					borderBottomLeftRadius: padBorderRadius( bottomLeft ),
 					borderBottomRightRadius: padBorderRadius( bottomRight ),
+					...styles,
 				};
 			}
 
@@ -361,12 +387,10 @@ export default function SearchEdit( {
 				? `${ borderRadius }px`
 				: borderRadius;
 
-			return {
-				borderRadius: `calc(${ radius } + ${ DEFAULT_INNER_PADDING })`,
-			};
+			styles.borderRadius = `calc(${ radius } + ${ DEFAULT_INNER_PADDING })`;
 		}
 
-		return undefined;
+		return styles;
 	};
 
 	const blockProps = useBlockProps( {
@@ -392,7 +416,10 @@ export default function SearchEdit( {
 				size={ {
 					width: `${ width }${ widthUnit }`,
 				} }
-				className="wp-block-search__inside-wrapper"
+				className={ classnames(
+					'wp-block-search__inside-wrapper',
+					isButtonPositionInside ? borderProps.className : undefined
+				) }
 				style={ getWrapperStyles() }
 				minWidth={ MIN_WIDTH }
 				enable={ getResizableSides() }
@@ -411,16 +438,15 @@ export default function SearchEdit( {
 				} }
 				showHandle={ isSelected }
 			>
-				{ ( 'button-inside' === buttonPosition ||
-					'button-outside' === buttonPosition ) && (
+				{ ( isButtonPositionInside || isButtonPositionOutside ) && (
 					<>
 						{ renderTextField() }
 						{ renderButton() }
 					</>
 				) }
 
-				{ 'button-only' === buttonPosition && renderButton() }
-				{ 'no-button' === buttonPosition && renderTextField() }
+				{ hasOnlyButton && renderButton() }
+				{ hasNoButton && renderTextField() }
 			</ResizableBox>
 		</div>
 	);
diff --git a/packages/block-library/src/search/index.php b/packages/block-library/src/search/index.php
index 2b6d74d52a1c0e..9014bf7f990a79 100644
--- a/packages/block-library/src/search/index.php
+++ b/packages/block-library/src/search/index.php
@@ -27,16 +27,20 @@ function render_block_core_search( $attributes ) {
 		)
 	);
 
-	$input_id        = 'wp-block-search__input-' . ++$instance_id;
-	$classnames      = classnames_for_block_core_search( $attributes );
-	$show_label      = ( ! empty( $attributes['showLabel'] ) ) ? true : false;
-	$use_icon_button = ( ! empty( $attributes['buttonUseIcon'] ) ) ? true : false;
-	$show_input      = ( ! empty( $attributes['buttonPosition'] ) && 'button-only' === $attributes['buttonPosition'] ) ? false : true;
-	$show_button     = ( ! empty( $attributes['buttonPosition'] ) && 'no-button' === $attributes['buttonPosition'] ) ? false : true;
-	$label_markup    = '';
-	$input_markup    = '';
-	$button_markup   = '';
-	$inline_styles   = styles_for_block_core_search( $attributes );
+	$input_id         = 'wp-block-search__input-' . ++$instance_id;
+	$classnames       = classnames_for_block_core_search( $attributes );
+	$show_label       = ( ! empty( $attributes['showLabel'] ) ) ? true : false;
+	$use_icon_button  = ( ! empty( $attributes['buttonUseIcon'] ) ) ? true : false;
+	$show_input       = ( ! empty( $attributes['buttonPosition'] ) && 'button-only' === $attributes['buttonPosition'] ) ? false : true;
+	$show_button      = ( ! empty( $attributes['buttonPosition'] ) && 'no-button' === $attributes['buttonPosition'] ) ? false : true;
+	$label_markup     = '';
+	$input_markup     = '';
+	$button_markup    = '';
+	$inline_styles    = styles_for_block_core_search( $attributes );
+	$is_button_inside = ! empty( $attributes['buttonPosition'] ) &&
+		'button-inside' === $attributes['buttonPosition'];
+	// Border color classes need to be applied to the elements that have a border color.
+	$border_color_classes = get_border_color_classes_for_block_core_search( $attributes );
 
 	if ( $show_label ) {
 		if ( ! empty( $attributes['label'] ) ) {
@@ -55,9 +59,11 @@ function render_block_core_search( $attributes ) {
 	}
 
 	if ( $show_input ) {
-		$input_markup = sprintf(
-			'<input type="search" id="%s" class="wp-block-search__input" name="s" value="%s" placeholder="%s" %s required />',
+		$input_classes = ! $is_button_inside ? $border_color_classes : '';
+		$input_markup  = sprintf(
+			'<input type="search" id="%s" class="wp-block-search__input %s" name="s" value="%s" placeholder="%s" %s required />',
 			$input_id,
+			$input_classes,
 			esc_attr( get_search_query() ),
 			esc_attr( $attributes['placeholder'] ),
 			$inline_styles['shared']
@@ -66,14 +72,14 @@ function render_block_core_search( $attributes ) {
 
 	if ( $show_button ) {
 		$button_internal_markup = '';
-		$button_classes         = '';
+		$button_classes         = ! $is_button_inside ? $border_color_classes : '';
 
 		if ( ! $use_icon_button ) {
 			if ( ! empty( $attributes['buttonText'] ) ) {
 				$button_internal_markup = $attributes['buttonText'];
 			}
 		} else {
-			$button_classes        .= 'has-icon';
+			$button_classes        .= ' has-icon';
 			$button_internal_markup =
 				'<svg id="search-icon" class="search-icon" viewBox="0 0 24 24" width="24" height="24">
 			        <path d="M13.5 6C10.5 6 8 8.5 8 11.5c0 1.1.3 2.1.9 3l-3.4 3 1 1.1 3.4-2.9c1 .9 2.2 1.4 3.6 1.4 3 0 5.5-2.5 5.5-5.5C19 8.5 16.5 6 13.5 6zm0 9.5c-2.2 0-4-1.8-4-4s1.8-4 4-4 4 1.8 4 4-1.8 4-4 4z"></path>
@@ -81,19 +87,21 @@ function render_block_core_search( $attributes ) {
 		}
 
 		$button_markup = sprintf(
-			'<button type="submit" class="wp-block-search__button %s"%s>%s</button>',
+			'<button type="submit" class="wp-block-search__button %s" %s>%s</button>',
 			$button_classes,
 			$inline_styles['shared'],
 			$button_internal_markup
 		);
 	}
 
-	$field_markup       = sprintf(
-		'<div class="wp-block-search__inside-wrapper"%s>%s</div>',
+	$field_markup_classes = $is_button_inside ? $border_color_classes : '';
+	$field_markup         = sprintf(
+		'<div class="wp-block-search__inside-wrapper %s" %s>%s</div>',
+		$field_markup_classes,
 		$inline_styles['wrapper'],
 		$input_markup . $button_markup
 	);
-	$wrapper_attributes = get_block_wrapper_attributes( array( 'class' => $classnames ) );
+	$wrapper_attributes   = get_block_wrapper_attributes( array( 'class' => $classnames ) );
 
 	return sprintf(
 		'<form role="search" method="get" action="%s" %s>%s</form>',
@@ -190,7 +198,8 @@ function styles_for_block_core_search( $attributes ) {
 	if ( $has_border_radius ) {
 		$default_padding = '4px';
 		$border_radius   = $attributes['style']['border']['radius'];
-		$button_inside   = ! empty( $attributes['buttonPosition'] ) &&
+		// Apply wrapper border radius if button placed inside.
+		$is_button_inside = ! empty( $attributes['buttonPosition'] ) &&
 			'button-inside' === $attributes['buttonPosition'];
 
 		if ( is_array( $border_radius ) ) {
@@ -209,7 +218,7 @@ function styles_for_block_core_search( $attributes ) {
 
 					// Add adjusted border radius styles for the wrapper element
 					// if button is positioned inside.
-					if ( $button_inside && intval( $value ) !== 0 ) {
+					if ( $is_button_inside && intval( $value ) !== 0 ) {
 						$wrapper_styles[] = sprintf(
 							'border-%s-radius: calc(%s + %s);',
 							esc_attr( $name ),
@@ -224,7 +233,7 @@ function styles_for_block_core_search( $attributes ) {
 			$border_radius   = is_numeric( $border_radius ) ? $border_radius . 'px' : $border_radius;
 			$shared_styles[] = sprintf( 'border-radius: %s;', esc_attr( $border_radius ) );
 
-			if ( $button_inside && intval( $border_radius ) !== 0 ) {
+			if ( $is_button_inside && intval( $border_radius ) !== 0 ) {
 				// Adjust wrapper border radii to maintain visual consistency
 				// with inner elements when button is positioned inside.
 				$wrapper_styles[] = sprintf(
@@ -236,8 +245,41 @@ function styles_for_block_core_search( $attributes ) {
 		}
 	}
 
+	// Add border color styles.
+	$has_border_color = ! empty( $attributes['style']['border']['color'] );
+
+	if ( $has_border_color ) {
+		$border_color     = $attributes['style']['border']['color'];
+		$is_button_inside = ! empty( $attributes['buttonPosition'] ) &&
+			'button-inside' === $attributes['buttonPosition'];
+
+		// Apply wrapper border color if button placed inside.
+		if ( $is_button_inside ) {
+			$wrapper_styles[] = sprintf( 'border-color: %s;', esc_attr( $border_color ) );
+		} else {
+			$shared_styles[] = sprintf( 'border-color: %s;', esc_attr( $border_color ) );
+		}
+	}
+
 	return array(
 		'shared'  => ! empty( $shared_styles ) ? sprintf( ' style="%s"', implode( ' ', $shared_styles ) ) : '',
 		'wrapper' => ! empty( $wrapper_styles ) ? sprintf( ' style="%s"', implode( ' ', $wrapper_styles ) ) : '',
 	);
 }
+
+/**
+ * Returns border color classnames depending on whether there are named or custom border colors.
+ *
+ * @param array $attributes The block attributes.
+ *
+ * @return string The border color classnames to be applied to the block elements.
+ */
+function get_border_color_classes_for_block_core_search( $attributes ) {
+	$has_custom_border_color = ! empty( $attributes['style']['border']['color'] );
+	$border_color_classes    = ! empty( $attributes['borderColor'] ) ? sprintf( 'has-border-color has-%s-border-color', $attributes['borderColor'] ) : '';
+	// If there's a border color style and no `borderColor` text string, we still want to add the generic `has-border-color` class name to the element.
+	if ( $has_custom_border_color && empty( $attributes['borderColor'] ) ) {
+		$border_color_classes = 'has-border-color';
+	}
+	return $border_color_classes;
+}