diff --git a/packages/e2e-tests/plugins/interactive-blocks/directive-on/render.php b/packages/e2e-tests/plugins/interactive-blocks/directive-on/render.php
index edb081922fc0e4..eb2de94ab58eea 100644
--- a/packages/e2e-tests/plugins/interactive-blocks/directive-on/render.php
+++ b/packages/e2e-tests/plugins/interactive-blocks/directive-on/render.php
@@ -51,4 +51,24 @@
 			data-wp-on--click="actions.clickHandler"
 		>Click me!</button>
 	</div>
+	<div data-wp-context='{"clicked":false,"clickCount":0,"isOpen":true}'>
+		<p
+			data-wp-text="context.clicked"
+			data-testid="multiple handlers clicked"
+		>false</p>
+		<p
+			data-wp-text="context.clickCount"
+			data-testid="multiple handlers clickCount"
+		>0</p>
+		<p
+			data-wp-text="context.isOpen"
+			data-testid="multiple handlers isOpen"
+		>true</p>
+		<button
+			data-testid="multiple handlers button"
+			data-wp-on--click="actions.setClicked"
+			data-wp-on--click--counter="actions.countClick"
+			data-wp-on--click--toggle="actions.toggle"
+		>Click me!</button>
+	</div>
 </div>
diff --git a/packages/e2e-tests/plugins/interactive-blocks/directive-on/view.js b/packages/e2e-tests/plugins/interactive-blocks/directive-on/view.js
index 69378b53e14c0a..8b0bcc0e115eca 100644
--- a/packages/e2e-tests/plugins/interactive-blocks/directive-on/view.js
+++ b/packages/e2e-tests/plugins/interactive-blocks/directive-on/view.js
@@ -26,5 +26,17 @@ const { state } = store( 'directive-on', {
 			const context = getContext();
 			context.customEvents += 1;
 		},
+		setClicked: () => {
+			const context = getContext();
+			context.clicked = true;
+		},
+		countClick: () => {
+			const context = getContext();
+			context.clickCount += 1;
+		},
+		toggle: () => {
+			const context = getContext();
+			context.isOpen = ! context.isOpen;
+		},
 	},
 } );
diff --git a/packages/interactivity/src/directives.js b/packages/interactivity/src/directives.js
index b19067bdc1ad9a..c20ea3aec722d3 100644
--- a/packages/interactivity/src/directives.js
+++ b/packages/interactivity/src/directives.js
@@ -270,13 +270,22 @@ export default () => {
 
 	// data-wp-on--[event]
 	directive( 'on', ( { directives: { on }, element, evaluate } ) => {
+		const events = new Map();
 		on.filter( ( { suffix } ) => suffix !== 'default' ).forEach(
 			( entry ) => {
-				element.props[ `on${ entry.suffix }` ] = ( event ) => {
-					evaluate( entry, event );
-				};
+				const event = entry.suffix.split( '--' )[ 0 ];
+				if ( ! events.has( event ) ) events.set( event, new Set() );
+				events.get( event ).add( entry );
 			}
 		);
+
+		events.forEach( ( entries, eventType ) => {
+			element.props[ `on${ eventType }` ] = ( event ) => {
+				entries.forEach( ( entry ) => {
+					evaluate( entry, event );
+				} );
+			};
+		} );
 	} );
 
 	// data-wp-on-window--[event]
diff --git a/test/e2e/specs/interactivity/directive-on.spec.ts b/test/e2e/specs/interactivity/directive-on.spec.ts
index 03dfe64462c567..886f74335e7aee 100644
--- a/test/e2e/specs/interactivity/directive-on.spec.ts
+++ b/test/e2e/specs/interactivity/directive-on.spec.ts
@@ -51,4 +51,29 @@ test.describe( 'data-wp-on', () => {
 			.click( { clickCount: 3, delay: 100 } );
 		await expect( counter ).toHaveText( '3' );
 	} );
+
+	test( 'should work with multiple event handlers on the same event type', async ( {
+		page,
+	} ) => {
+		const button = page.getByTestId( 'multiple handlers button' );
+		const isOpen = page.getByTestId( 'multiple handlers isOpen' );
+		const clicked = page.getByTestId( 'multiple handlers clicked' );
+		const clickCount = page.getByTestId( 'multiple handlers clickCount' );
+
+		await expect( clicked ).toHaveText( 'false' );
+		await expect( clickCount ).toHaveText( '0' );
+		await expect( isOpen ).toHaveText( 'true' );
+
+		await button.click();
+
+		await expect( clicked ).toHaveText( 'true' );
+		await expect( clickCount ).toHaveText( '1' );
+		await expect( isOpen ).toHaveText( 'false' );
+
+		await button.click();
+
+		await expect( clicked ).toHaveText( 'true' );
+		await expect( clickCount ).toHaveText( '2' );
+		await expect( isOpen ).toHaveText( 'true' );
+	} );
 } );