diff --git a/src/file-token-group/__tests__/file-token-group.test.tsx b/src/file-token-group/__tests__/file-token-group.test.tsx
index 22284f31ae..44349df3a0 100644
--- a/src/file-token-group/__tests__/file-token-group.test.tsx
+++ b/src/file-token-group/__tests__/file-token-group.test.tsx
@@ -212,8 +212,11 @@ describe('File loading', () => {
   test('Spinner added when loading', () => {
     const wrapper = render({ items: [{ file: file1, loading: true }, { file: file2 }] });
 
-    expect(wrapper.findFileToken(1)?.getElement().firstChild).toHaveClass(styles.loading);
-    expect(wrapper.findFileToken(2)?.getElement().firstChild).not.toHaveClass(styles.loading);
+    // Reach into the token-box since the file-token now composes InternalToken.
+    expect(wrapper.findFileToken(1)?.getElement().querySelector(`.${styles['token-box']}`)).toHaveClass(styles.loading);
+    expect(wrapper.findFileToken(2)?.getElement().querySelector(`.${styles['token-box']}`)).not.toHaveClass(
+      styles.loading
+    );
   });
 });
 
diff --git a/src/file-token-group/file-token.tsx b/src/file-token-group/file-token.tsx
index e2b1e6a904..d83e2befdd 100644
--- a/src/file-token-group/file-token.tsx
+++ b/src/file-token-group/file-token.tsx
@@ -11,7 +11,7 @@ import { FormFieldError, FormFieldWarning } from '../form-field/internal';
 import { BaseComponentProps } from '../internal/base-component/index.js';
 import InternalSpaceBetween from '../space-between/internal.js';
 import InternalSpinner from '../spinner/internal.js';
-import DismissButton from '../token/dismiss-button.js';
+import InternalToken from '../token/internal.js';
 import { TokenGroupProps } from '../token-group/interfaces.js';
 import Tooltip from '../tooltip/internal.js';
 import * as defaultFormatters from './default-formatters.js';
@@ -77,9 +77,7 @@ function InternalFileToken({
   const [showTooltip, setShowTooltip] = useState(false);
   const [isTruncated, setIsTruncated] = useState(false);
 
-  const getDismissLabel = (fileIndex: number) => {
-    return i18nStrings?.removeFileAriaLabel?.(fileIndex, file.name);
-  };
+  const getDismissLabel = (fileIndex: number) => i18nStrings?.removeFileAriaLabel?.(fileIndex, file.name);
 
   function isEllipsisActive() {
     const span = fileNameRef.current;
@@ -99,6 +97,76 @@ function InternalFileToken({
   const fileIsSingleRow =
     !showFileLastModified && !showFileSize && (!groupContainsImage || (groupContainsImage && !showFileThumbnail));
 
+  // The full body of the token. Rendered through InternalToken's customContent slot so this
+  // component owns the inner layout (thumbnail + metadata column + loading overlay), while
+  // InternalToken handles the token-box and the dismiss button.
+  const fileContent = (
+    <>
+      {loading && (
+        <div
+          className={clsx(styles['file-loading-overlay'], {
+            [styles['file-loading-overlay-single-row']]: loading && fileIsSingleRow,
+          })}
+        >
+          <InternalSpinner variant="normal" size="normal" />
+        </div>
+      )}
+      <InternalBox className={styles['file-option']}>
+        {showFileThumbnail && isImage && <FileOptionThumbnail file={file} />}
+
+        <div
+          className={clsx(styles['file-option-metadata'], {
+            [styles['with-image']]: showFileThumbnail && isImage,
+            [styles['single-row-loading']]: loading && fileIsSingleRow,
+          })}
+        >
+          <InternalSpaceBetween direction="vertical" size="xxxs">
+            <div
+              className={styles['file-name-container']}
+              onMouseOver={() => setShowTooltip(true)}
+              onMouseOut={() => setShowTooltip(false)}
+              onFocus={() => setShowTooltip(true)}
+              onBlur={() => setShowTooltip(false)}
+              role={isTruncated ? 'button' : undefined}
+              aria-expanded={isTruncated ? showTooltip : undefined}
+              tabIndex={isTruncated ? 0 : -1}
+              ref={fileNameContainerRef}
+            >
+              <InternalBox
+                fontWeight="normal"
+                className={clsx(styles['file-option-name'], testUtilStyles['file-option-name'], {
+                  [testUtilStyles['ellipsis-active']]: isTruncated,
+                })}
+              >
+                <span ref={fileNameRef}>{file.name}</span>
+              </InternalBox>
+            </div>
+
+            {showFileSize && file.size ? (
+              <InternalBox
+                fontSize="body-s"
+                color={'text-body-secondary'}
+                className={clsx(styles['file-option-size'], testUtilStyles['file-option-size'])}
+              >
+                {formatFileSize(file.size)}
+              </InternalBox>
+            ) : null}
+
+            {showFileLastModified && file.lastModified ? (
+              <InternalBox
+                fontSize="body-s"
+                color={'text-body-secondary'}
+                className={clsx(styles['file-option-last-modified'], testUtilStyles['file-option-last-modified'])}
+              >
+                {formatFileLastModified(new Date(file.lastModified))}
+              </InternalBox>
+            ) : null}
+          </InternalSpaceBetween>
+        </div>
+      </InternalBox>
+    </>
+  );
+
   return (
     <div
       ref={containerRef}
@@ -109,82 +177,24 @@ function InternalFileToken({
       role="group"
       aria-label={file.name}
       aria-describedby={errorText ? errorId : warningText ? warningId : undefined}
-      aria-disabled={loading}
+      aria-disabled={loading || undefined}
       data-index={index}
     >
-      <div
-        className={clsx(styles['token-box'], {
+      <InternalToken
+        // The outer wrapper above is the accessibility group (role="group" + aria-label). The
+        // token itself is presentation-only so screen readers don't see two nested groups.
+        role="presentation"
+        __customContent={fileContent}
+        onDismiss={readOnly ? undefined : onDismiss}
+        dismissLabel={getDismissLabel(index)}
+        __tokenBoxClassName={clsx(styles['token-box'], {
           [styles.loading]: loading,
           [styles.error]: errorText,
           [styles.warning]: showWarning,
           [styles.horizontal]: alignment === 'horizontal',
           [styles['read-only']]: readOnly,
         })}
-      >
-        {loading && (
-          <div
-            className={clsx(styles['file-loading-overlay'], {
-              [styles['file-loading-overlay-single-row']]: loading && fileIsSingleRow,
-            })}
-          >
-            <InternalSpinner variant="normal" size="normal" />
-          </div>
-        )}
-        <InternalBox className={styles['file-option']}>
-          {showFileThumbnail && isImage && <FileOptionThumbnail file={file} />}
-
-          <div
-            className={clsx(styles['file-option-metadata'], {
-              [styles['with-image']]: showFileThumbnail && isImage,
-              [styles['single-row-loading']]: loading && fileIsSingleRow,
-            })}
-          >
-            <InternalSpaceBetween direction="vertical" size="xxxs">
-              <div
-                className={styles['file-name-container']}
-                onMouseOver={() => setShowTooltip(true)}
-                onMouseOut={() => setShowTooltip(false)}
-                onFocus={() => setShowTooltip(true)}
-                onBlur={() => setShowTooltip(false)}
-                role={isTruncated ? 'button' : undefined}
-                aria-expanded={isTruncated ? showTooltip : undefined}
-                tabIndex={isTruncated ? 0 : -1}
-                ref={fileNameContainerRef}
-              >
-                <InternalBox
-                  fontWeight="normal"
-                  className={clsx(styles['file-option-name'], testUtilStyles['file-option-name'], {
-                    [testUtilStyles['ellipsis-active']]: isTruncated,
-                  })}
-                >
-                  <span ref={fileNameRef}>{file.name}</span>
-                </InternalBox>
-              </div>
-
-              {showFileSize && file.size ? (
-                <InternalBox
-                  fontSize="body-s"
-                  color={'text-body-secondary'}
-                  className={clsx(styles['file-option-size'], testUtilStyles['file-option-size'])}
-                >
-                  {formatFileSize(file.size)}
-                </InternalBox>
-              ) : null}
-
-              {showFileLastModified && file.lastModified ? (
-                <InternalBox
-                  fontSize="body-s"
-                  color={'text-body-secondary'}
-                  className={clsx(styles['file-option-last-modified'], testUtilStyles['file-option-last-modified'])}
-                >
-                  {formatFileLastModified(new Date(file.lastModified))}
-                </InternalBox>
-              ) : null}
-            </InternalSpaceBetween>
-          </div>
-        </InternalBox>
-        {onDismiss && !readOnly && <DismissButton dismissLabel={getDismissLabel(index)} onDismiss={onDismiss} />}
-      </div>
+      />
       {errorText && (
         <FormFieldError id={errorId} errorIconAriaLabel={i18nStrings?.errorIconAriaLabel}>
           {errorText}
diff --git a/src/token/internal.tsx b/src/token/internal.tsx
index 8d7bede72e..e04170430f 100644
--- a/src/token/internal.tsx
+++ b/src/token/internal.tsx
@@ -28,10 +28,25 @@ import analyticsSelectors from './analytics-metadata/styles.css.js';
 import styles from './styles.css.js';
 import testUtilStyles from './test-classes/styles.css.js';
 
-type InternalTokenProps = TokenProps &
+type InternalTokenProps = Omit<TokenProps, 'label'> &
   InternalBaseComponentProps & {
+    /** Token label. Required unless `__customContent` replaces the option layout entirely. */
+    label?: React.ReactNode;
+    /**
+     * Overrides the default `role="group"` on the token root. Set to `"presentation"` when a
+     * parent element provides grouping semantics; this also strips ARIA attributes
+     * (aria-label, aria-labelledby, aria-disabled), focus/mouse handlers, and the tab stop so the
+     * token doesn't expose a redundant nested group to assistive tech.
+     */
     role?: string;
     disableInnerPadding?: boolean;
+    /** Extra class on the token-box element */
+    __tokenBoxClassName?: string;
+    /**
+     * Renders content inside the token-box, replacing the standard option layout
+     * (label, labelTag, description, tags). The dismiss button is still rendered as a sibling.
+     */
+    __customContent?: React.ReactNode;
   };
 
 function InternalToken({
@@ -52,6 +67,8 @@ function InternalToken({
   // Internal
   role,
   disableInnerPadding,
+  __tokenBoxClassName,
+  __customContent,
 
   // Base
   __internalRootRef,
@@ -65,6 +82,9 @@ function InternalToken({
   const [isEllipsisActive, setIsEllipsisActive] = useState(false);
   const isInline = variant === 'inline';
   const isOneTheme = isThemeActive(Theme.OneTheme);
+  // Consumers with their own grouping semantics can pass role="presentation" to treat the root
+  // as a pure styling wrapper (strips ARIA and focus/mouse handlers).
+  const isPresentation = role === 'presentation';
   const ariaLabelledbyId = useUniqueId();
 
   const isLabelOverflowing = () => {
@@ -131,23 +151,31 @@ function InternalToken({
           analyticsSelectors.token,
           baseProps.className
         )}
-        aria-label={ariaLabel}
-        aria-labelledby={!ariaLabel ? ariaLabelledbyId : undefined}
-        aria-disabled={!!disabled}
+        aria-label={isPresentation ? undefined : ariaLabel}
+        aria-labelledby={isPresentation || ariaLabel ? undefined : ariaLabelledbyId}
+        aria-disabled={isPresentation ? undefined : !!disabled}
         role={role ?? 'group'}
         onFocus={() => {
-          setShowTooltip(true);
+          if (!isPresentation) {
+            setShowTooltip(true);
+          }
         }}
         onBlur={() => {
-          setShowTooltip(false);
+          if (!isPresentation) {
+            setShowTooltip(false);
+          }
         }}
         onMouseEnter={() => {
-          setShowTooltip(true);
+          if (!isPresentation) {
+            setShowTooltip(true);
+          }
         }}
         onMouseLeave={() => {
-          setShowTooltip(false);
+          if (!isPresentation) {
+            setShowTooltip(false);
+          }
         }}
-        tabIndex={!!tooltipContent && isInline && isEllipsisActive ? 0 : undefined}
+        tabIndex={!isPresentation && !!tooltipContent && isInline && isEllipsisActive ? 0 : undefined}
       >
         <SpanOrDivTag
           className={clsx(
@@ -155,7 +183,8 @@ function InternalToken({
             disabled && styles['token-box-disabled'],
             readOnly && styles['token-box-readonly'],
             !isInline && !onDismiss && styles['token-box-without-dismiss'],
-            disableInnerPadding && styles['disable-padding']
+            disableInnerPadding && styles['disable-padding'],
+            __tokenBoxClassName
           )}
           style={tokenRootStyleProps}
         >
@@ -167,6 +196,7 @@ function InternalToken({
             labelContainerRef={labelContainerRef}
             labelRef={labelRef}
             labelId={ariaLabelledbyId}
+            customContent={__customContent}
           />
           {onDismiss && (
             <DismissButton