diff --git a/src/lib/spacing.tsx b/src/lib/spacing.tsx
index 780d9a9472..3af60cdc1a 100644
--- a/src/lib/spacing.tsx
+++ b/src/lib/spacing.tsx
@@ -1,5 +1,5 @@
 import { Children, HTMLAttributes, HTMLProps, ReactNode } from 'react';
-import styled from 'styled-components';
+import styled, { css } from 'styled-components';
 import { Box, BoxComponentProps } from './components/box/Box';
 
 export const spacing = {
@@ -33,39 +33,89 @@ export const spacing = {
   f40: '40px',
 };
 
-const HSeparator = styled.div`
-  background: ${(props) => props.theme.border};
+// The two separator treatments. A row Stack draws a full-height rule between
+// its children; a column Stack draws a short dash. They are different shapes,
+// not one shape on two axes, so a single element cannot serve both by CSS alone
+// — which is why `stackBelow` below restyles the element rather than relying on
+// the flip.
+const ruleSeparator = css`
   width: 1px;
   align-self: stretch;
   flex-shrink: 0;
-  margin: ${spacing.r12} 0px;
+  margin: ${spacing.r12} 0;
 `;
 
-const VSeparator = styled.div`
-  height: 1px;
+const dashSeparator = css`
   width: ${spacing.r24};
+  height: 1px;
+  align-self: auto;
+  margin: 0;
+`;
+
+// One element for both directions. `Stack` used to pick between two components
+// at render time, which meant a CSS direction change left the separators
+// pointing the wrong way — CSS can restyle an element but cannot swap which one
+// React rendered.
+const Separator = styled.div<{
+  $direction: 'vertical' | 'horizontal';
+  $stackBelow?: number;
+}>`
   background: ${(props) => props.theme.border};
+  ${(props) =>
+    props.$direction === 'horizontal' ? ruleSeparator : dashSeparator}
+
+  ${(props) =>
+    props.$direction === 'horizontal' &&
+    props.$stackBelow !== undefined &&
+    css`
+      @container responsive (max-width: ${props.$stackBelow}px) {
+        ${dashSeparator}
+      }
+    `}
 `;
 
-const Separator = ({ type }: { type?: 'vertical' | 'horizontal' }) => {
-  return (
-    <>
-      {type === 'horizontal' && <HSeparator>&nbsp;</HSeparator>}
-      {type === 'vertical' && <VSeparator>&nbsp;</VSeparator>}
-    </>
-  );
-};
+// Layout lives here rather than on `Box`'s props so the container query below
+// isn't fighting styled-system output for specificity.
+const StackBox = styled(Box)<{
+  $direction: 'vertical' | 'horizontal';
+  $stackBelow?: number;
+}>`
+  display: flex;
+  flex-direction: ${(props) =>
+    props.$direction === 'horizontal' ? 'row' : 'column'};
+  align-items: ${(props) =>
+    props.$direction === 'horizontal' ? 'center' : 'normal'};
+
+  ${(props) =>
+    props.$direction === 'horizontal' &&
+    props.$stackBelow !== undefined &&
+    css`
+      @container responsive (max-width: ${props.$stackBelow}px) {
+        flex-direction: column;
+        align-items: normal;
+      }
+    `}
+`;
 
 export const Stack = ({
   gap,
   direction,
   withSeparators,
+  stackBelow,
   children,
   ...rest
 }: {
   gap?: keyof typeof spacing;
   direction?: 'vertical' | 'horizontal';
   withSeparators?: boolean;
+  /**
+   * Below this container width (px) a horizontal Stack becomes vertical, and
+   * its separators become the vertical treatment along with it. Requires an
+   * ancestor that establishes the `responsive` container — `<Box container>`.
+   * Without one the query never matches and the Stack stays horizontal.
+   * Ignored when `direction="vertical"`.
+   */
+  stackBelow?: number;
   children: ReactNode[];
   container?: boolean;
 } & HTMLAttributes<HTMLDivElement>) => {
@@ -75,10 +125,9 @@ export const Stack = ({
   const numberOfChildren = Children.count(children);
 
   return (
-    <Box
-      display={'flex'}
-      flexDirection={direction === 'horizontal' ? 'row' : 'column'}
-      alignItems={direction === 'horizontal' ? 'center' : 'normal'}
+    <StackBox
+      $direction={direction}
+      $stackBelow={stackBelow}
       gap={spacing[gap]}
       {...rest}
     >
@@ -87,12 +136,12 @@ export const Stack = ({
           <>
             {node}
             {withSeparators && nodeIndex + 1 !== numberOfChildren && (
-              <Separator type={direction} />
+              <Separator $direction={direction} $stackBelow={stackBelow} />
             )}
           </>
         );
       })}
-    </Box>
+    </StackBox>
   );
 };
 
diff --git a/stories/spacing.stories.tsx b/stories/spacing.stories.tsx
index 16e1ab04df..38cdd0bcca 100644
--- a/stories/spacing.stories.tsx
+++ b/stories/spacing.stories.tsx
@@ -1,5 +1,5 @@
 import React from 'react';
-import { useTheme } from 'styled-components';
+import styled, { useTheme } from 'styled-components';
 import { Icon } from '../src/lib/components/icon/Icon.component';
 import {
   EmphaseText,
@@ -113,6 +113,64 @@ export const StackStory = {
   },
 };
 
+// `stackBelow` queries the `responsive` container, so an ancestor has to
+// establish one. `<Box container>` does this in app code.
+const ResizableContainer = styled.div`
+  container-type: inline-size;
+  container-name: responsive;
+  resize: horizontal;
+  overflow: auto;
+  min-width: 240px;
+  max-width: 100%;
+  width: 700px;
+  background: ${(props) => props.theme.backgroundLevel2};
+  padding: ${spacing.r16};
+`;
+
+export const StackBelowStory = {
+  name: 'stackBelow — direction follows the container width',
+  render: ({}) => (
+    <>
+      <h2>Drag the bottom-right handle below 500px</h2>
+      <SecondaryText>
+        One prop. The Stack flips from row to column in CSS only — no re-render
+        — and the separators switch from the row treatment (a full-height rule)
+        to the column treatment (a short dash) along with it.
+      </SecondaryText>
+      <ResizableContainer>
+        <Stack withSeparators gap="r24" stackBelow={500}>
+          <Stack gap="r16">
+            <Icon name="Account" size="2x" color="infoPrimary" withWrapper />
+            <Stack direction="vertical" gap="r4">
+              <LargerText>12</LargerText>
+              <SmallerSecondaryText>Accounts</SmallerSecondaryText>
+            </Stack>
+          </Stack>
+          <Stack gap="r16">
+            <Icon name="Bucket" size="2x" color="infoPrimary" withWrapper />
+            <Stack direction="vertical" gap="r4">
+              <LargerText>148</LargerText>
+              <SmallerSecondaryText>Buckets</SmallerSecondaryText>
+            </Stack>
+          </Stack>
+          <Stack gap="r16">
+            <Icon
+              name="Node-backend"
+              size="2x"
+              color="infoPrimary"
+              withWrapper
+            />
+            <Stack direction="vertical" gap="r4">
+              <LargerText>3</LargerText>
+              <SmallerSecondaryText>Endpoints</SmallerSecondaryText>
+            </Stack>
+          </Stack>
+        </Stack>
+      </ResizableContainer>
+    </>
+  ),
+};
+
 export const WrapStory = {
   render: ({}) => {
     const theme = useTheme();