diff --git a/packages/components/CHANGELOG.md b/packages/components/CHANGELOG.md
index 2a6102335c2f6..9b02dfe344aa9 100644
--- a/packages/components/CHANGELOG.md
+++ b/packages/components/CHANGELOG.md
@@ -18,6 +18,7 @@
 -   Fixed race conditions causing conditionally displayed `ToolsPanelItem` components to be erroneously deregistered ([#36588](https://github.com/WordPress/gutenberg/pull/36588)).
 -   Added `__experimentalHideHeader` prop to `Modal` component ([#36831](https://github.com/WordPress/gutenberg/pull/36831)).
 -   Added experimental `ConfirmDialog` component ([#34153](https://github.com/WordPress/gutenberg/pull/34153)).
+-   Divider: improve support for vertical orientation and RTL styles, use start/end logical props instead of top/bottom, change border-color to `currentColor` ([#36579](https://github.com/WordPress/gutenberg/pull/36579)).
 
 ### Bug Fix
 
diff --git a/packages/components/src/card/test/__snapshots__/index.js.snap b/packages/components/src/card/test/__snapshots__/index.js.snap
index adf11cff8056a..ca20d69a5c18d 100644
--- a/packages/components/src/card/test/__snapshots__/index.js.snap
+++ b/packages/components/src/card/test/__snapshots__/index.js.snap
@@ -269,10 +269,10 @@ Object {
 }
 
 .emotion-10 {
-  border-color: rgba(0, 0, 0, 0.1);
-  border-width: 0 0 1px 0;
-  height: 0;
+  border: 0;
   margin: 0;
+  border-bottom: 1px solid currentColor;
+  height: 0;
   width: auto;
   box-sizing: border-box;
   display: block;
@@ -525,10 +525,10 @@ Object {
 }
 
 .emotion-10 {
-  border-color: rgba(0, 0, 0, 0.1);
-  border-width: 0 0 1px 0;
-  height: 0;
+  border: 0;
   margin: 0;
+  border-bottom: 1px solid currentColor;
+  height: 0;
   width: auto;
   box-sizing: border-box;
   display: block;
diff --git a/packages/components/src/divider/README.md b/packages/components/src/divider/README.md
index ae9b961dad5e5..977f969d40ff5 100644
--- a/packages/components/src/divider/README.md
+++ b/packages/components/src/divider/README.md
@@ -9,15 +9,43 @@ This feature is still experimental. “Experimental” means this is an early im
 ## Usage
 
 ```jsx
-import { Divider, FormGroup, ListGroup } from '@wordpress/components/ui';
+import {
+	__experimentalDivider as Divider,
+	__experimentalText as Text,
+	__experimentalVStack as VStack,
+} from `@wordpress/components`;
 
 function Example() {
 	return (
-		<ListGroup>
-			<FormGroup>...</FormGroup>
+		<VStack spacing={4}>
+			<Text>Some text here</Text>
 			<Divider />
-			<FormGroup>...</FormGroup>
-		</ListGroup>
+			<Text>Some more text here</Text>
+		</VStack>
 	);
 }
 ```
+
+## Props
+
+### `margin`: `number`
+
+Adjusts all margins on the inline dimension.
+
+- Required: No
+
+### `marginStart`: `number`
+
+Adjusts the inline-start margin.
+
+- Required: No
+
+### `marginEnd`: `number`
+
+Adjusts the inline-end margin.
+
+- Required: No
+
+### Inherited props
+
+`Divider` also inherits all of the [`Separator` props](https://reakit.io/docs/separator/).
diff --git a/packages/components/src/divider/component.tsx b/packages/components/src/divider/component.tsx
index 085d2f5f012b7..15a61adab5c2a 100644
--- a/packages/components/src/divider/component.tsx
+++ b/packages/components/src/divider/component.tsx
@@ -38,17 +38,18 @@ function Divider(
  * @example
  * ```js
  * import {
- *     __experimentalDivider as Divider,
- *     __experimentalText as Text }
- * from `@wordpress/components`;
+ * 		__experimentalDivider as Divider,
+ * 		__experimentalText as Text,
+ * 		__experimentalVStack as VStack,
+ * } from `@wordpress/components`;
  *
  * function Example() {
  * 	return (
- * 		<ListGroup>
- * 			<FormGroup>...</FormGroup>
+ * 		<VStack spacing={4}>
+ * 			<Text>Some text here</Text>
  * 			<Divider />
- * 			<FormGroup>...</FormGroup>
- * 		</ListGroup>
+ * 			<Text>Some more text here</Text>
+ * 		</VStack>
  * 	);
  * }
  * ```
diff --git a/packages/components/src/divider/stories/index.js b/packages/components/src/divider/stories/index.js
index a3a7b595db3bf..a721007068aaa 100644
--- a/packages/components/src/divider/stories/index.js
+++ b/packages/components/src/divider/stories/index.js
@@ -1,38 +1,64 @@
 /**
  * External dependencies
  */
-import { number } from '@storybook/addon-knobs';
+import { css } from '@emotion/react';
 
 /**
  * Internal dependencies
  */
+import { useCx } from '../../utils';
+import { Text } from '../../text';
 import { Divider } from '..';
 
 export default {
 	component: Divider,
 	title: 'Components (Experimental)/Divider',
-	parameters: {
-		knobs: { disabled: false },
+	argTypes: {
+		margin: {
+			control: { type: 'number' },
+		},
+		marginStart: {
+			control: { type: 'number' },
+		},
+		marginEnd: {
+			control: { type: 'number' },
+		},
 	},
 };
 
-const BlackDivider = ( props ) => (
-	<Divider { ...props } style={ { borderColor: 'black' } } />
+const HorizontalTemplate = ( args ) => (
+	<div>
+		<Text>Some text before the divider</Text>
+		<Divider { ...args } />
+		<Text>Some text after the divider</Text>
+	</div>
 );
 
-export const _default = () => {
-	const props = {
-		margin: number( 'margin', 0 ),
-	};
-	// make the border color black to give higher contrast and help it appear in storybook better
-	return <BlackDivider { ...props } />;
+const VerticalTemplate = ( args ) => {
+	const cx = useCx();
+	const wrapperClassName = cx( css`
+		display: flex;
+		align-items: stretch;
+		justify-content: start;
+	` );
+
+	return (
+		<div className={ wrapperClassName }>
+			<Text>Some text before the divider</Text>
+			<Divider orientation="vertical" { ...args } />
+			<Text>Some text after the divider</Text>
+		</div>
+	);
 };
 
-export const splitMargins = () => {
-	const props = {
-		marginTop: number( 'marginTop', 0 ),
-		marginBottom: number( 'marginBottom', 0 ),
-	};
+export const Horizontal = HorizontalTemplate.bind( {} );
+Horizontal.args = {
+	margin: 2,
+	marginStart: undefined,
+	marginEnd: undefined,
+};
 
-	return <BlackDivider { ...props } />;
+export const Vertical = VerticalTemplate.bind( {} );
+Vertical.args = {
+	...Horizontal.args,
 };
diff --git a/packages/components/src/divider/styles.ts b/packages/components/src/divider/styles.ts
index 270cc27cd80a0..50b4934211802 100644
--- a/packages/components/src/divider/styles.ts
+++ b/packages/components/src/divider/styles.ts
@@ -8,29 +8,66 @@ import { css } from '@emotion/react';
  * Internal dependencies
  */
 import { space } from '../ui/utils/space';
-import CONFIG from '../utils/config-values';
-import type { OwnProps } from './types';
+import { rtl } from '../utils';
+import type { Props } from './types';
 
-const renderMargin = ( { margin, marginTop, marginBottom }: OwnProps ) => {
-	if ( typeof margin !== 'undefined' ) {
-		return css( {
-			marginBottom: space( margin ),
-			marginTop: space( margin ),
-		} );
-	}
+const MARGIN_DIRECTIONS: Record<
+	NonNullable< Props[ 'orientation' ] >,
+	Record< 'start' | 'end', string >
+> = {
+	vertical: {
+		start: 'marginLeft',
+		end: 'marginRight',
+	},
+	horizontal: {
+		start: 'marginTop',
+		end: 'marginBottom',
+	},
+};
+
+// Renders the correct margins given the Divider's `orientation` and the writing direction.
+// When both the generic `margin` and the specific `marginStart|marginEnd` props are defined,
+// the latter will take priority.
+const renderMargin = ( {
+	'aria-orientation': orientation = 'horizontal',
+	margin,
+	marginStart,
+	marginEnd,
+}: Props ) =>
+	css(
+		rtl( {
+			[ MARGIN_DIRECTIONS[ orientation ].start ]: space(
+				marginStart ?? margin
+			),
+			[ MARGIN_DIRECTIONS[ orientation ].end ]: space(
+				marginEnd ?? margin
+			),
+		} )()
+	);
 
+const renderBorder = ( {
+	'aria-orientation': orientation = 'horizontal',
+}: Props ) => {
 	return css( {
-		marginTop: space( marginTop ),
-		marginBottom: space( marginBottom ),
+		[ orientation === 'vertical'
+			? 'borderRight'
+			: 'borderBottom' ]: '1px solid currentColor',
 	} );
 };
 
-export const DividerView = styled.hr< OwnProps >`
-	border-color: ${ CONFIG.colorDivider };
-	border-width: 0 0 1px 0;
-	height: 0;
+const renderSize = ( {
+	'aria-orientation': orientation = 'horizontal',
+}: Props ) =>
+	css( {
+		height: orientation === 'vertical' ? 'auto' : 0,
+		width: orientation === 'vertical' ? 0 : 'auto',
+	} );
+
+export const DividerView = styled.hr< Props >`
+	border: 0;
 	margin: 0;
-	width: auto;
 
+	${ renderBorder }
+	${ renderSize }
 	${ renderMargin }
 `;
diff --git a/packages/components/src/divider/test/__snapshots__/index.js.snap b/packages/components/src/divider/test/__snapshots__/index.js.snap
index d19ce16daf39c..5a330d602a560 100644
--- a/packages/components/src/divider/test/__snapshots__/index.js.snap
+++ b/packages/components/src/divider/test/__snapshots__/index.js.snap
@@ -2,10 +2,10 @@
 
 exports[`props should render correctly 1`] = `
 .emotion-0 {
-  border-color: rgba(0, 0, 0, 0.1);
-  border-width: 0 0 1px 0;
-  height: 0;
+  border: 0;
   margin: 0;
+  border-bottom: 1px solid currentColor;
+  height: 0;
   width: auto;
 }
 
@@ -25,8 +25,8 @@ Snapshot Diff:
 
 @@ -2,10 +2,8 @@
     Object {
-      "border-color": "rgba(0, 0, 0, 0.1)",
-      "border-width": "0 0 1px 0",
+      "border": "0",
+      "border-bottom": "1px solid currentColor",
       "height": "0",
       "margin": "0",
 -     "margin-bottom": "calc(4px * 7)",
@@ -36,15 +36,15 @@ Snapshot Diff:
   ]
 `;
 
-exports[`props should render marginBottom 1`] = `
+exports[`props should render marginEnd 1`] = `
 Snapshot Diff:
 - Received styles
 + Base styles
 
 @@ -2,9 +2,8 @@
     Object {
-      "border-color": "rgba(0, 0, 0, 0.1)",
-      "border-width": "0 0 1px 0",
+      "border": "0",
+      "border-bottom": "1px solid currentColor",
       "height": "0",
       "margin": "0",
 -     "margin-bottom": "calc(4px * 5)",
@@ -53,15 +53,15 @@ Snapshot Diff:
   ]
 `;
 
-exports[`props should render marginTop 1`] = `
+exports[`props should render marginStart 1`] = `
 Snapshot Diff:
 - Received styles
 + Base styles
 
 @@ -2,9 +2,8 @@
     Object {
-      "border-color": "rgba(0, 0, 0, 0.1)",
-      "border-width": "0 0 1px 0",
+      "border": "0",
+      "border-bottom": "1px solid currentColor",
       "height": "0",
       "margin": "0",
 -     "margin-top": "calc(4px * 5)",
diff --git a/packages/components/src/divider/test/index.js b/packages/components/src/divider/test/index.js
index 239206a5f5442..424fa33ce368b 100644
--- a/packages/components/src/divider/test/index.js
+++ b/packages/components/src/divider/test/index.js
@@ -18,15 +18,15 @@ describe( 'props', () => {
 		expect( base.container.firstChild ).toMatchSnapshot();
 	} );
 
-	test( 'should render marginTop', () => {
-		const { container } = render( <Divider marginTop={ 5 } /> );
+	test( 'should render marginStart', () => {
+		const { container } = render( <Divider marginStart={ 5 } /> );
 		expect( container.firstChild ).toMatchStyleDiffSnapshot(
 			base.container.firstChild
 		);
 	} );
 
-	test( 'should render marginBottom', () => {
-		const { container } = render( <Divider marginBottom={ 5 } /> );
+	test( 'should render marginEnd', () => {
+		const { container } = render( <Divider marginEnd={ 5 } /> );
 		expect( container.firstChild ).toMatchStyleDiffSnapshot(
 			base.container.firstChild
 		);
diff --git a/packages/components/src/divider/types.ts b/packages/components/src/divider/types.ts
index 70a17881cc0e6..e531aa0561afd 100644
--- a/packages/components/src/divider/types.ts
+++ b/packages/components/src/divider/types.ts
@@ -11,17 +11,17 @@ import type { SpaceInput } from '../ui/utils/space';
 
 export interface OwnProps {
 	/**
-	 * Adjusts all margins.
+	 * Adjusts all margins on the inline dimension.
 	 */
 	margin?: SpaceInput;
 	/**
-	 * Adjusts top margins.
+	 * Adjusts the inline-start margin.
 	 */
-	marginTop?: SpaceInput;
+	marginStart?: SpaceInput;
 	/**
-	 * Adjusts bottom margins.
+	 * Adjusts the inline-end margin.
 	 */
-	marginBottom?: SpaceInput;
+	marginEnd?: SpaceInput;
 }
 
 export interface Props extends Omit< SeparatorProps, 'children' >, OwnProps {}