diff --git a/build-tools/utils/custom-css-properties.js b/build-tools/utils/custom-css-properties.js
index 8f8225825c..895243883a 100644
--- a/build-tools/utils/custom-css-properties.js
+++ b/build-tools/utils/custom-css-properties.js
@@ -95,6 +95,9 @@ const customCssPropertiesList = [
   'styleBoxShadowDefault',
   'styleBoxShadowDisabled',
   'styleBoxShadowHover',
+  'stylePaddingInline',
+  'stylePaddingInlineStart',
+  'stylePaddingInlineEnd',
   // Readonly state
   'styleBackgroundReadonly',
   'styleBorderColorReadonly',
diff --git a/src/input/__tests__/styles.test.tsx b/src/input/__tests__/styles.test.tsx
index b209b6a2d6..187d629c19 100644
--- a/src/input/__tests__/styles.test.tsx
+++ b/src/input/__tests__/styles.test.tsx
@@ -2,12 +2,40 @@
 // SPDX-License-Identifier: Apache-2.0
 import customCssProps from '../../internal/generated/custom-css-properties';
 import { getInputStyles } from '../styles';
+import { parsePaddingInline } from '../utils';
 
 // Mock the environment module
 jest.mock('../../internal/environment', () => ({
   SYSTEM: 'core',
 }));
 
+describe('parsePaddingInline', () => {
+  test('returns undefined for both start and end when input is undefined', () => {
+    expect(parsePaddingInline(undefined)).toEqual({ start: undefined, end: undefined });
+  });
+
+  test('handles single value - applies to both start and end', () => {
+    expect(parsePaddingInline('10px')).toEqual({ start: '10px', end: '10px' });
+    expect(parsePaddingInline('1rem')).toEqual({ start: '1rem', end: '1rem' });
+    expect(parsePaddingInline('0')).toEqual({ start: '0', end: '0' });
+  });
+
+  test('handles shorthand notation - first value is start, second is end', () => {
+    expect(parsePaddingInline('10px 20px')).toEqual({ start: '10px', end: '20px' });
+    expect(parsePaddingInline('1rem 2rem')).toEqual({ start: '1rem', end: '2rem' });
+    expect(parsePaddingInline('5px 10px')).toEqual({ start: '5px', end: '10px' });
+  });
+
+  test('handles extra whitespace', () => {
+    expect(parsePaddingInline('  10px  20px  ')).toEqual({ start: '10px', end: '20px' });
+    expect(parsePaddingInline('10px    20px')).toEqual({ start: '10px', end: '20px' });
+  });
+
+  test('ignores values beyond the first two', () => {
+    expect(parsePaddingInline('10px 20px 30px 40px')).toEqual({ start: '10px', end: '20px' });
+  });
+});
+
 describe('getInputStyles', () => {
   afterEach(() => {
     jest.resetModules();
@@ -68,7 +96,9 @@ describe('getInputStyles', () => {
       fontSize: '14px',
       fontWeight: '400',
       paddingBlock: '8px',
-      paddingInline: '12px',
+      [customCssProps.stylePaddingInline]: '12px',
+      [customCssProps.stylePaddingInlineStart]: '12px',
+      [customCssProps.stylePaddingInlineEnd]: '12px',
       [customCssProps.styleBackgroundDefault]: '#ffffff',
       [customCssProps.styleBackgroundDisabled]: '#f0f0f0',
       [customCssProps.styleBackgroundHover]: '#fafafa',
@@ -96,6 +126,55 @@ describe('getInputStyles', () => {
     });
   });
 
+  test('handles shorthand paddingInline values correctly', () => {
+    const styleWithShorthand = {
+      root: {
+        paddingInline: '10px 20px',
+      },
+    };
+
+    const result = getInputStyles(styleWithShorthand);
+
+    expect(result).toEqual({
+      [customCssProps.stylePaddingInline]: '10px 20px',
+      [customCssProps.stylePaddingInlineStart]: '10px',
+      [customCssProps.stylePaddingInlineEnd]: '20px',
+    });
+  });
+
+  test('handles single value paddingInline correctly', () => {
+    const styleWithSingleValue = {
+      root: {
+        paddingInline: '15px',
+      },
+    };
+
+    const result = getInputStyles(styleWithSingleValue);
+
+    expect(result).toEqual({
+      [customCssProps.stylePaddingInline]: '15px',
+      [customCssProps.stylePaddingInlineStart]: '15px',
+      [customCssProps.stylePaddingInlineEnd]: '15px',
+    });
+  });
+
+  test('does not add padding properties when paddingInline is not provided', () => {
+    const styleWithoutPadding = {
+      root: {
+        fontSize: '14px',
+      },
+    };
+
+    const result = getInputStyles(styleWithoutPadding);
+
+    expect(result).toEqual({
+      fontSize: '14px',
+    });
+    expect(result).not.toHaveProperty(customCssProps.stylePaddingInline);
+    expect(result).not.toHaveProperty(customCssProps.stylePaddingInlineStart);
+    expect(result).not.toHaveProperty(customCssProps.stylePaddingInlineEnd);
+  });
+
   test('returns undefined when SYSTEM is not core', async () => {
     jest.resetModules();
     jest.doMock('../../internal/environment', () => ({
diff --git a/src/input/styles.scss b/src/input/styles.scss
index e6b3856ac1..154261e544 100644
--- a/src/input/styles.scss
+++ b/src/input/styles.scss
@@ -34,7 +34,7 @@
 .input {
   @include styles.styles-reset;
   padding-block: styles.$control-padding-vertical;
-  padding-inline: styles.$control-padding-horizontal;
+  padding-inline: var(#{custom-props.$stylePaddingInline}, #{styles.$control-padding-horizontal});
   color: var(#{custom-props.$styleColorDefault}, awsui.$color-text-body-default);
   inline-size: 100%;
   cursor: text;
@@ -128,9 +128,12 @@
   &.input-invalid {
     @include styles.form-invalid-control();
     &.input-has-icon-left {
-      padding-inline-start: calc(
-        #{styles.$control-icon-horizontal-padding} -
-          (#{styles.$invalid-control-left-border} - #{awsui.$border-width-field})
+      padding-inline-start: max(
+        var(#{custom-props.$stylePaddingInlineStart}, #{styles.$control-padding-horizontal}),
+        calc(
+          #{styles.$control-icon-horizontal-padding} -
+            (#{styles.$invalid-control-left-border} - #{awsui.$border-width-field})
+        )
       );
     }
   }
@@ -138,9 +141,12 @@
   &.input-warning {
     @include styles.form-warning-control();
     &.input-has-icon-left {
-      padding-inline-start: calc(
-        #{styles.$control-icon-horizontal-padding} -
-          (#{styles.$invalid-control-left-border} - #{awsui.$border-width-field})
+      padding-inline-start: max(
+        var(#{custom-props.$stylePaddingInlineStart}, #{styles.$control-padding-horizontal}),
+        calc(
+          #{styles.$control-icon-horizontal-padding} -
+            (#{styles.$invalid-control-left-border} - #{awsui.$border-width-field})
+        )
       );
     }
   }
@@ -159,10 +165,16 @@
     }
   }
   &.input-has-icon-left {
-    padding-inline-start: styles.$control-icon-horizontal-padding;
+    padding-inline-start: max(
+      var(#{custom-props.$stylePaddingInlineStart}, #{styles.$control-padding-horizontal}),
+      #{styles.$control-icon-horizontal-padding}
+    );
   }
   &.input-has-icon-right {
-    padding-inline-end: styles.$control-icon-horizontal-padding;
+    padding-inline-end: max(
+      var(#{custom-props.$stylePaddingInlineEnd}, #{styles.$control-padding-horizontal}),
+      #{styles.$control-icon-horizontal-padding}
+    );
   }
   &.input-has-no-border-radius {
     border-start-start-radius: awsui.$border-radius-dropdown;
diff --git a/src/input/styles.tsx b/src/input/styles.tsx
index f0e17cf567..c873f0288d 100644
--- a/src/input/styles.tsx
+++ b/src/input/styles.tsx
@@ -3,18 +3,32 @@
 import { SYSTEM } from '../internal/environment';
 import customCssProps from '../internal/generated/custom-css-properties';
 import { InputProps } from './interfaces';
+import { parsePaddingInline } from './utils';
 
 export function getInputStyles(style: InputProps['style']) {
   let properties = {};
 
   if (style?.root && SYSTEM === 'core') {
+    // We are only supporting logical shorthand properties for padding (e.g. "10px 30px"),
+    // so wen ened to deconstruct this into start- and end-padding to be able to style
+    // them separately.
+    const { start: paddingStart, end: paddingEnd } = parsePaddingInline(style?.root?.paddingInline);
+
     properties = {
       borderRadius: style?.root?.borderRadius,
       borderWidth: style?.root?.borderWidth,
       fontSize: style?.root?.fontSize,
       fontWeight: style?.root?.fontWeight,
       paddingBlock: style?.root?.paddingBlock,
-      paddingInline: style?.root?.paddingInline,
+      ...(style?.root?.paddingInline && {
+        [customCssProps.stylePaddingInline]: style.root.paddingInline,
+      }),
+      ...(paddingStart && {
+        [customCssProps.stylePaddingInlineStart]: paddingStart,
+      }),
+      ...(paddingEnd && {
+        [customCssProps.stylePaddingInlineEnd]: paddingEnd,
+      }),
       ...(style?.root?.backgroundColor && {
         [customCssProps.styleBackgroundDefault]: style.root.backgroundColor?.default,
         [customCssProps.styleBackgroundDisabled]: style.root.backgroundColor?.disabled,
diff --git a/src/input/utils.ts b/src/input/utils.ts
index 88518aa9cd..be45a5fb50 100644
--- a/src/input/utils.ts
+++ b/src/input/utils.ts
@@ -37,3 +37,18 @@ export const convertAutoComplete = (propertyValue: boolean | string = false): st
   }
   return propertyValue || 'off';
 };
+
+/**
+ * Parses CSS paddingInline value into separate start and end values.
+ * Handles both single values ('10px') and shorthand notation ('10px 20px').
+ */
+export const parsePaddingInline = (
+  paddingInline: string | undefined
+): { start: string | undefined; end: string | undefined } => {
+  if (!paddingInline) {
+    return { start: undefined, end: undefined };
+  }
+
+  const [start, end = start] = paddingInline.trim().split(/\s+/);
+  return { start, end };
+};