diff --git a/pages/popover/style-api-v2.page.tsx b/pages/popover/style-api-v2.page.tsx
new file mode 100644
index 0000000000..ee43cf2e0c
--- /dev/null
+++ b/pages/popover/style-api-v2.page.tsx
@@ -0,0 +1,64 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+import React, { useContext } from 'react';
+
+import { Checkbox, KeyValuePairs, Popover } from '~components';
+
+import AppContext, { AppContextType } from '../app/app-context';
+import { SimplePage } from '../app/templates';
+
+import styles from './style-api-v2.scss';
+
+const brand = { popover: styles['popover-brand'], dismissButton: styles['popover-brand-dismiss'] };
+
+type PageContext = React.Context<
+  AppContextType<{
+    renderWithPortal: boolean;
+  }>
+>;
+
+export default function () {
+  const {
+    urlParams: { renderWithPortal = true },
+    setUrlParams,
+  } = useContext(AppContext as PageContext);
+  const shared = { header: 'Popover header', content: 'Popover content', renderWithPortal };
+  return (
+    <SimplePage
+      title="Popover - Style API v2"
+      screenshotArea={{}}
+      settings={
+        <Checkbox
+          checked={renderWithPortal}
+          onChange={({ detail }) => setUrlParams({ renderWithPortal: detail.checked })}
+        >
+          renderWithPortal
+        </Checkbox>
+      }
+    >
+      <KeyValuePairs
+        columns={4}
+        items={[
+          {
+            type: 'pair',
+            label: 'Brand',
+            value: (
+              <Popover {...shared} {...{ styleClassNames: brand }}>
+                Open popover
+              </Popover>
+            ),
+          },
+          {
+            type: 'pair',
+            label: 'Borderless',
+            value: (
+              <Popover {...shared} {...{ styleClassNames: { popover: styles['popover-borderless'] } }}>
+                Open popover
+              </Popover>
+            ),
+          },
+        ]}
+      />
+    </SimplePage>
+  );
+}
diff --git a/pages/popover/style-api-v2.scss b/pages/popover/style-api-v2.scss
new file mode 100644
index 0000000000..50293a238a
--- /dev/null
+++ b/pages/popover/style-api-v2.scss
@@ -0,0 +1,29 @@
+/*
+ Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+ SPDX-License-Identifier: Apache-2.0
+*/
+
+@use '../style-api/palette' as palette;
+
+.popover-brand {
+  --awsui-style-color: #{palette.$genai-text};
+  --awsui-style-background: #{palette.$genai-surface};
+  --awsui-style-border-color: #{palette.$genai};
+  --awsui-style-border-width: 3px;
+  --awsui-style-border-radius: 8px;
+}
+
+.popover-borderless {
+  --awsui-style-background: #{palette.$subtle};
+  --awsui-style-border-width: 0px;
+  --awsui-style-border-radius: 4px;
+}
+
+.popover-brand-dismiss {
+  --awsui-style-color: #{palette.$genai};
+  --awsui-style-focus-ring-color: #{palette.$genai};
+
+  &:hover {
+    --awsui-style-color: #{palette.$genai-hover};
+  }
+}
diff --git a/pages/tooltip/style-api-v2.page.tsx b/pages/tooltip/style-api-v2.page.tsx
new file mode 100644
index 0000000000..f1823835bd
--- /dev/null
+++ b/pages/tooltip/style-api-v2.page.tsx
@@ -0,0 +1,36 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+import React, { useRef, useState } from 'react';
+
+import { Button, Tooltip } from '~components';
+
+import { SimplePage } from '../app/templates';
+
+import styles from './style-api-v2.scss';
+
+export default function () {
+  const triggerRef = useRef<HTMLSpanElement>(null);
+  const [open, setOpen] = useState(false);
+  return (
+    <SimplePage title="Tooltip - Style API v2" screenshotArea={{}}>
+      <br />
+      <span
+        ref={triggerRef}
+        onMouseEnter={() => setOpen(true)}
+        onMouseLeave={() => setOpen(false)}
+        onFocus={() => setOpen(true)}
+        onBlur={() => setOpen(false)}
+      >
+        <Button variant="icon" iconName="copy" ariaLabel="Copy" />
+        {open && (
+          <Tooltip
+            content="ARN Copied"
+            getTrack={() => triggerRef.current}
+            onEscape={() => setOpen(false)}
+            {...{ styleClassNames: { tooltip: styles['tooltip-inverted'] } }}
+          />
+        )}
+      </span>
+    </SimplePage>
+  );
+}
diff --git a/pages/tooltip/style-api-v2.scss b/pages/tooltip/style-api-v2.scss
new file mode 100644
index 0000000000..6abb52a76b
--- /dev/null
+++ b/pages/tooltip/style-api-v2.scss
@@ -0,0 +1,13 @@
+/*
+ Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+ SPDX-License-Identifier: Apache-2.0
+*/
+
+@use '../style-api/palette' as palette;
+
+.tooltip-inverted {
+  --awsui-style-color: #{palette.$text-on-accent};
+  --awsui-style-background: #{palette.$accent};
+  --awsui-style-border-color: #{palette.$accent};
+  --awsui-style-border-radius: 2px;
+}
diff --git a/src/__tests__/snapshot-tests/__snapshots__/style-docs.test.ts.snap b/src/__tests__/snapshot-tests/__snapshots__/style-docs.test.ts.snap
index 0ec1499e58..54e5e0a134 100644
--- a/src/__tests__/snapshot-tests/__snapshots__/style-docs.test.ts.snap
+++ b/src/__tests__/snapshot-tests/__snapshots__/style-docs.test.ts.snap
@@ -174,6 +174,36 @@ exports[`Style API docs definition for link matches the snapshot: link 1`] = `
 }
 `;
 
+exports[`Style API docs definition for popover matches the snapshot: popover 1`] = `
+{
+  "slots": [
+    {
+      "name": "popover",
+      "properties": [],
+      "propertyDescriptions": {},
+      "tokenDescriptions": {
+        "background": "Background of the surface and arrow.",
+        "border-color": "Border color of the surface and arrow.",
+        "border-width": "Border width of the surface and arrow.",
+      },
+      "tokens": [
+        "background",
+        "border-color",
+        "border-width",
+        "border-radius",
+      ],
+    },
+    {
+      "forwardsTo": {
+        "component": "button",
+        "slot": "root",
+      },
+      "name": "dismissButton",
+    },
+  ],
+}
+`;
+
 exports[`Style API docs definition for radio-button matches the snapshot: radio-button 1`] = `
 {
   "slots": [
@@ -237,6 +267,29 @@ exports[`Style API docs definition for toggle matches the snapshot: toggle 1`] =
 }
 `;
 
+exports[`Style API docs definition for tooltip matches the snapshot: tooltip 1`] = `
+{
+  "slots": [
+    {
+      "name": "tooltip",
+      "properties": [],
+      "propertyDescriptions": {},
+      "tokenDescriptions": {
+        "background": "Background of the surface and arrow.",
+        "border-color": "Border color of the surface and arrow.",
+        "border-width": "Border width of the surface and arrow.",
+      },
+      "tokens": [
+        "background",
+        "border-color",
+        "border-width",
+        "border-radius",
+      ],
+    },
+  ],
+}
+`;
+
 exports[`Style API docs list of components with a Style API doc matches the snapshot 1`] = `
 [
   "alert",
@@ -245,7 +298,9 @@ exports[`Style API docs list of components with a Style API doc matches the snap
   "checkbox",
   "dropdown",
   "link",
+  "popover",
   "radio-button",
   "toggle",
+  "tooltip",
 ]
 `;
diff --git a/src/internal/styles/style-api.scss b/src/internal/styles/style-api.scss
index a245639edf..8e3a8eddfd 100644
--- a/src/internal/styles/style-api.scss
+++ b/src/internal/styles/style-api.scss
@@ -51,9 +51,9 @@ $_focus-ring-carriers: toolkit.resolve($focus-ring, carrier);
   }
 }
 
-@mixin docs($name, $map) {
+@mixin docs($name, $tokens: null, $properties: null, $descriptions: null) {
   @if enabled() {
-    @include toolkit.docs($name, $map);
+    @include toolkit.docs($name, $tokens, $properties, $descriptions);
   }
 }
 
diff --git a/src/popover/__tests__/style-api.test.tsx b/src/popover/__tests__/style-api.test.tsx
new file mode 100644
index 0000000000..f324417ae9
--- /dev/null
+++ b/src/popover/__tests__/style-api.test.tsx
@@ -0,0 +1,40 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+import React from 'react';
+import { render } from '@testing-library/react';
+
+import Popover from '../../../lib/components/popover';
+import createWrapper from '../../../lib/components/test-utils/dom';
+
+import styles from '../../../lib/components/popover/styles.css.js';
+
+function renderOpenPopover(props: Record<string, unknown>) {
+  const { container } = render(<Popover content="Content" header="Header" {...props} />);
+  const wrapper = createWrapper(container).findPopover()!;
+  wrapper.findTrigger().click();
+  return wrapper;
+}
+
+describe('Popover Style API v2', () => {
+  test('applies styleClassNames to the popover container', () => {
+    const wrapper = renderOpenPopover({ styleClassNames: { popover: 'a', unknown: 'b' } });
+    expect(wrapper.findByClassName(styles.container)!.getElement()).toHaveClass('a');
+    expect(wrapper.find('.b')).toBeNull();
+  });
+
+  test('forwards the dismissButton slot to the dismiss button', () => {
+    const wrapper = renderOpenPopover({ styleClassNames: { dismissButton: 'a' } });
+    expect(wrapper.findDismissButton()!.getElement()).toHaveClass('a');
+  });
+
+  test('applies styleClassNames to the popover container when rendered in a portal', () => {
+    const wrapper = renderOpenPopover({ renderWithPortal: true, styleClassNames: { popover: 'a' } });
+    expect(wrapper.findContent({ renderWithPortal: true })).not.toBeNull();
+    expect(document.body.querySelector(`.${styles.container}`)).toHaveClass('a');
+  });
+
+  test('does not leak the styleClassNames prop to the DOM', () => {
+    renderOpenPopover({ renderWithPortal: true, styleClassNames: { popover: 'a' } });
+    expect(document.body.querySelector('[styleClassNames]')).toBeNull();
+  });
+});
diff --git a/src/popover/arrow.scss b/src/popover/arrow.scss
index 15b3f0a42c..4038762cb8 100644
--- a/src/popover/arrow.scss
+++ b/src/popover/arrow.scss
@@ -3,6 +3,8 @@
 
 @use '../internal/styles' as styles;
 @use '../internal/styles/tokens' as awsui;
+@use '../internal/styles/style-api' as style-api;
+@use './style-api' as popover-style-api;
 
 .arrow {
   // Arrow design:
@@ -64,19 +66,22 @@
 
   &-outer {
     &::after {
-      background-color: awsui.$color-border-popover;
+      background-color: style-api.value(popover-style-api.$tokens, border-color, awsui.$color-border-popover);
     }
   }
 
   &-inner {
-    inset-block-start: calc(awsui.$border-width-popover + 1px);
+    // The inner triangle is shifted by the border width plus up to 1px so that the uncovered part of the
+    // outer triangle renders as the border; min() collapses the shift to 0 for a borderless popover.
+    $border-width: style-api.value(popover-style-api.$tokens, border-width, awsui.$border-width-popover);
+    inset-block-start: calc(#{$border-width} + min(#{$border-width}, 1px));
 
     &::after {
       border-start-start-radius: 1px;
       border-start-end-radius: 0;
       border-end-start-radius: 0;
       border-end-end-radius: 0;
-      background-color: awsui.$color-background-popover;
+      background: style-api.value(popover-style-api.$tokens, background, awsui.$color-background-popover);
     }
   }
 
diff --git a/src/popover/body.scss b/src/popover/body.scss
index f9633f4cf0..6e44477919 100644
--- a/src/popover/body.scss
+++ b/src/popover/body.scss
@@ -9,6 +9,7 @@ $header-row-margin-block-end: awsui.$space-xs;
 .body {
   @include styles.styles-reset;
   @include styles.text-flex-wrapping;
+  color: awsui.$color-text-body-default;
 
   padding-block: awsui.$space-s;
   padding-inline: awsui.$space-m;
diff --git a/src/popover/body.tsx b/src/popover/body.tsx
index 8bca2d3cf1..69e1c35582 100644
--- a/src/popover/body.tsx
+++ b/src/popover/body.tsx
@@ -28,6 +28,7 @@ export interface PopoverBodyProps {
   overflowVisible?: 'content' | 'both';
 
   className?: string;
+  dismissButtonClassName?: string;
   ariaLabelledby?: string;
 
   closeAnalyticsAction?: string;
@@ -46,6 +47,7 @@ const PopoverBody = React.forwardRef(
       variant,
       overflowVisible,
       className,
+      dismissButtonClassName,
       ariaLabelledby,
       closeAnalyticsAction,
     }: PopoverBodyProps,
@@ -90,6 +92,7 @@ const PopoverBody = React.forwardRef(
           ariaLabel={i18n('dismissAriaLabel', dismissAriaLabel)}
           onClick={() => onDismiss?.('close-button')}
           ref={dismissButtonRef}
+          styleClassNames={{ root: dismissButtonClassName }}
         />
       </div>
     );
diff --git a/src/popover/container.scss b/src/popover/container.scss
index 6f91714b2e..74a242fbd9 100644
--- a/src/popover/container.scss
+++ b/src/popover/container.scss
@@ -3,6 +3,8 @@
 
 @use '../internal/styles' as styles;
 @use '../internal/styles/tokens' as awsui;
+@use '../internal/styles/style-api' as style-api;
+@use './style-api' as popover-style-api;
 
 $arrow-height: 10px;
 
@@ -12,6 +14,7 @@ $arrow-height: 10px;
   inset-block-start: -9999px;
   inset-inline-start: -9999px;
   z-index: 2000;
+  @include style-api.carriers(popover-style-api.$tokens);
 
   // A little pseudoelement to extend the container to the space between the
   // popover and the trigger to avoid hover-based popovers/tooltips from
@@ -61,15 +64,18 @@ $arrow-height: 10px;
 }
 
 .container-body {
+  $tokens: popover-style-api.$tokens;
   @include styles.styles-reset;
-  border-start-start-radius: awsui.$border-radius-popover;
-  border-start-end-radius: awsui.$border-radius-popover;
-  border-end-start-radius: awsui.$border-radius-popover;
-  border-end-end-radius: awsui.$border-radius-popover;
-  background-color: awsui.$color-background-popover;
+  border-start-start-radius: style-api.value($tokens, border-radius, awsui.$border-radius-popover);
+  border-start-end-radius: style-api.value($tokens, border-radius, awsui.$border-radius-popover);
+  border-end-start-radius: style-api.value($tokens, border-radius, awsui.$border-radius-popover);
+  border-end-end-radius: style-api.value($tokens, border-radius, awsui.$border-radius-popover);
+  background: style-api.value($tokens, background, awsui.$color-background-popover);
   box-shadow: awsui.$shadow-popover;
-  border-block: awsui.$border-width-popover solid awsui.$color-border-popover;
-  border-inline: awsui.$border-width-popover solid awsui.$color-border-popover;
+  $border: style-api.value($tokens, border-width, awsui.$border-width-popover) solid
+    style-api.value($tokens, border-color, awsui.$color-border-popover);
+  border-block: $border;
+  border-inline: $border;
 }
 
 .container-body-variant-annotation {
diff --git a/src/popover/internal.tsx b/src/popover/internal.tsx
index f473552b63..7b5bf894c8 100644
--- a/src/popover/internal.tsx
+++ b/src/popover/internal.tsx
@@ -33,6 +33,13 @@ export interface InternalPopoverProps extends Omit<PopoverProps, 'triggerType' |
   isInline?: boolean;
   __visible?: boolean;
   __onVisibleChange?: NonCancelableEventHandler<{ visible: boolean }>;
+  styleClassNames?: StyleClassNames;
+}
+
+// Style API v2
+interface StyleClassNames {
+  popover?: string;
+  dismissButton?: string;
 }
 
 export default React.forwardRef(InternalPopover);
@@ -59,6 +66,7 @@ function InternalPopover(
     __closeAnalyticsAction,
     __visible: controlledVisible,
     __onVisibleChange: onVisibleChange,
+    styleClassNames,
 
     ...restProps
   }: InternalPopoverProps,
@@ -180,6 +188,7 @@ function InternalPopover(
         arrow={position => <Arrow position={position} />}
         renderWithPortal={renderWithPortal}
         zIndex={renderWithPortal ? 7000 : undefined}
+        className={styleClassNames?.popover}
       >
         <LinkDefaultVariantContext.Provider value={{ defaultVariant: 'primary' }}>
           <PopoverBody
@@ -187,6 +196,7 @@ function InternalPopover(
             dismissAriaLabel={dismissAriaLabel}
             header={header}
             onDismiss={onDismiss}
+            dismissButtonClassName={styleClassNames?.dismissButton}
             overflowVisible="both"
             closeAnalyticsAction={__closeAnalyticsAction}
           >
diff --git a/src/popover/style-api.scss b/src/popover/style-api.scss
new file mode 100644
index 0000000000..9ab0e31415
--- /dev/null
+++ b/src/popover/style-api.scss
@@ -0,0 +1,13 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+
+@use '../internal/styles/style-api' as style-api;
+
+// Style API v2 tokens of the popover surface, shared by Popover and Tooltip.
+$tokens: style-api.resolve((background, border-color, border-width, border-radius), carrier);
+
+$token-descriptions: (
+  background: 'Background of the surface and arrow.',
+  border-color: 'Border color of the surface and arrow.',
+  border-width: 'Border width of the surface and arrow.',
+);
diff --git a/src/popover/styles.scss b/src/popover/styles.scss
index 89a179b17c..68ad682313 100644
--- a/src/popover/styles.scss
+++ b/src/popover/styles.scss
@@ -7,11 +7,22 @@
 @use '../internal/styles/tokens' as awsui;
 @use '@cloudscape-design/component-toolkit/internal/focus-visible' as focus-visible;
 
+@use '../internal/styles/style-api' as style-api;
+@use './style-api' as popover-style-api;
+
 @use './arrow';
 @use './body';
 @use './container';
 @use './motion';
 
+@include style-api.register(popover-style-api.$tokens);
+@include style-api.docs(
+  'popover',
+  popover-style-api.$tokens,
+  $descriptions: (tokens: popover-style-api.$token-descriptions)
+);
+@include style-api.docs-forward('dismissButton', 'button', 'root');
+
 $trigger-underline-offset: 0.25em;
 
 .root {
diff --git a/src/tooltip/__tests__/style-api.test.tsx b/src/tooltip/__tests__/style-api.test.tsx
new file mode 100644
index 0000000000..2edf29bbee
--- /dev/null
+++ b/src/tooltip/__tests__/style-api.test.tsx
@@ -0,0 +1,27 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+import React from 'react';
+import { render } from '@testing-library/react';
+
+import Tooltip from '../../../lib/components/tooltip';
+
+import popoverStyles from '../../../lib/components/popover/styles.css.js';
+
+function renderTooltip(props: Record<string, unknown>) {
+  const trigger = document.createElement('button');
+  document.body.appendChild(trigger);
+  return render(<Tooltip content="Content" getTrack={() => trigger} {...props} />);
+}
+
+describe('Tooltip Style API v2', () => {
+  test('applies styleClassNames to the tooltip container', () => {
+    renderTooltip({ styleClassNames: { tooltip: 'a', unknown: 'b' } });
+    expect(document.body.querySelector(`.${popoverStyles.container}`)).toHaveClass('a');
+    expect(document.body.querySelector('.b')).toBeNull();
+  });
+
+  test('does not leak the styleClassNames prop to the DOM', () => {
+    renderTooltip({ styleClassNames: { tooltip: 'a' } });
+    expect(document.body.querySelector('[styleClassNames]')).toBeNull();
+  });
+});
diff --git a/src/tooltip/internal.tsx b/src/tooltip/internal.tsx
index 7556612d1d..d2ae9e30df 100644
--- a/src/tooltip/internal.tsx
+++ b/src/tooltip/internal.tsx
@@ -22,8 +22,14 @@ type InternalTooltipComponentProps = InternalTooltipProps &
     // ID of the associated trigger. When the trigger and the tooltip are connected via referrer ID, the
     // nodeBelongs(triggerNode, tooltipNode) returns true.
     referrerId?: string;
+    styleClassNames?: StyleClassNames;
   };
 
+// Style API v2
+interface StyleClassNames {
+  tooltip?: string;
+}
+
 export default function InternalTooltip({
   content,
   getTrack,
@@ -31,6 +37,7 @@ export default function InternalTooltip({
   position = 'top',
   onEscape,
   referrerId,
+  styleClassNames,
   __internalRootRef,
   ...restProps
 }: InternalTooltipComponentProps) {
@@ -86,7 +93,7 @@ export default function InternalTooltip({
               zIndex={7000}
               arrow={position => <PopoverArrow position={position} />}
               hideOnOverscroll={true}
-              className={className}
+              className={clsx(className, styleClassNames?.tooltip)}
             >
               <PopoverBody dismissButton={false} dismissAriaLabel={undefined} onDismiss={undefined} header={undefined}>
                 {content}
diff --git a/src/tooltip/styles.scss b/src/tooltip/styles.scss
index 65b7808010..f0e501b820 100644
--- a/src/tooltip/styles.scss
+++ b/src/tooltip/styles.scss
@@ -5,6 +5,14 @@
 
 @use '../internal/styles' as styles;
 @use '../internal/styles/tokens' as awsui;
+@use '../internal/styles/style-api' as style-api;
+@use '../popover/style-api' as popover-style-api;
+
+@include style-api.docs(
+  'tooltip',
+  popover-style-api.$tokens,
+  $descriptions: (tokens: popover-style-api.$token-descriptions)
+);
 
 .root {
   @include styles.with-motion {