diff --git a/packages/x-data-grid/src/components/columnHeaders/GridColumnHeaderItem.tsx b/packages/x-data-grid/src/components/columnHeaders/GridColumnHeaderItem.tsx
index ca3ed2a60b8ac..bfd22a0b5dbeb 100644
--- a/packages/x-data-grid/src/components/columnHeaders/GridColumnHeaderItem.tsx
+++ b/packages/x-data-grid/src/components/columnHeaders/GridColumnHeaderItem.tsx
@@ -38,6 +38,8 @@ interface GridColumnHeaderItemProps {
   indexInSection: number;
   sectionLength: number;
   gridHasFiller: boolean;
+  isLastUnpinned: boolean;
+  isSiblingFocused: boolean;
 }
 
 type OwnerState = GridColumnHeaderItemProps & {
@@ -56,6 +58,8 @@ const useUtilityClasses = (ownerState: OwnerState) => {
     showLeftBorder,
     filterItemsCounter,
     pinnedPosition,
+    isLastUnpinned,
+    isSiblingFocused,
   } = ownerState;
 
   const isColumnSorted = sortDirection != null;
@@ -79,6 +83,10 @@ const useUtilityClasses = (ownerState: OwnerState) => {
       showLeftBorder && 'columnHeader--withLeftBorder',
       pinnedPosition === 'left' && 'columnHeader--pinnedLeft',
       pinnedPosition === 'right' && 'columnHeader--pinnedRight',
+      // TODO: Remove classes below and restore `:has` selectors when they are supported in jsdom
+      // See https://github.com/mui/mui-x/pull/14559
+      isLastUnpinned && 'columnHeader--lastUnpinned',
+      isSiblingFocused && 'columnHeader--siblingFocused',
     ],
     draggableContainer: ['columnHeaderDraggableContainer'],
     titleContainer: ['columnHeaderTitleContainer'],
@@ -326,7 +334,9 @@ GridColumnHeaderItem.propTypes = {
   indexInSection: PropTypes.number.isRequired,
   isDragging: PropTypes.bool.isRequired,
   isLast: PropTypes.bool.isRequired,
+  isLastUnpinned: PropTypes.bool.isRequired,
   isResizing: PropTypes.bool.isRequired,
+  isSiblingFocused: PropTypes.bool.isRequired,
   pinnedPosition: PropTypes.oneOf(['left', 'right']),
   sectionLength: PropTypes.number.isRequired,
   separatorSide: PropTypes.oneOf(['left', 'right']),
diff --git a/packages/x-data-grid/src/components/containers/GridRootStyles.ts b/packages/x-data-grid/src/components/containers/GridRootStyles.ts
index 0c574a7bf3c72..3d1e28b943794 100644
--- a/packages/x-data-grid/src/components/containers/GridRootStyles.ts
+++ b/packages/x-data-grid/src/components/containers/GridRootStyles.ts
@@ -289,12 +289,10 @@ export const GridRootStyles = styled('div', {
     // - the column has a left or right border
     // - the next column is pinned right and has a left border
     [`& .${c.columnHeader}:focus,
-      & .${c.columnHeader}:focus-within,
-      & .${c.columnHeader}:has(+ .${c.columnHeader}:focus),
-      & .${c.columnHeader}:has(+ .${c.columnHeader}:focus-within),
       & .${c['columnHeader--withLeftBorder']},
       & .${c['columnHeader--withRightBorder']},
-      & .${c.columnHeader}:has(+ .${c.filler} + .${c['columnHeader--withLeftBorder']}),
+      & .${c['columnHeader--siblingFocused']},
+      & .${c['virtualScroller--hasScrollX']} .${c['columnHeader--lastUnpinned']},
       & .${c['virtualScroller--hasScrollX']} .${c['columnHeader--last']}
       `]: {
       [`& .${c.columnSeparator}`]: {
@@ -413,9 +411,7 @@ export const GridRootStyles = styled('div', {
     '@media (hover: none)': {
       [`& .${c.columnHeader}`]: columnHeaderStyles,
       [`& .${c.columnHeader}:focus,
-        & .${c.columnHeader}:focus-within,
-        & .${c.columnHeader}:has(+ .${c.columnHeader}:focus),
-        & .${c.columnHeader}:has(+ .${c.columnHeader}:focus-within)`]: {
+        & .${c['columnHeader--siblingFocused']}`]: {
         [`.${c['columnSeparator--resizable']}`]: {
           color: (t.vars || t).palette.primary.main,
         },
diff --git a/packages/x-data-grid/src/constants/gridClasses.ts b/packages/x-data-grid/src/constants/gridClasses.ts
index 330723133d737..ca4ed8ad672f9 100644
--- a/packages/x-data-grid/src/constants/gridClasses.ts
+++ b/packages/x-data-grid/src/constants/gridClasses.ts
@@ -163,6 +163,17 @@ export interface GridClasses {
    * Styles applied to the last column header element.
    */
   'columnHeader--last': string;
+  /**
+   * Styles applied to the last unpinned column header item.
+   * @ignore - do not document.
+   */
+  'columnHeader--lastUnpinned': string;
+  /**
+   * Styles applied to a column header item when its sibling with a bordering separator is focused.
+   * @ignore - do not document.
+   */
+  'columnHeader--siblingFocused': string;
+
   /**
    * Styles applied to the header checkbox cell element.
    */
@@ -686,6 +697,8 @@ export const gridClasses = generateUtilityClasses<GridClassKey>('MuiDataGrid', [
   'columnHeader--pinnedLeft',
   'columnHeader--pinnedRight',
   'columnHeader--last',
+  'columnHeader--lastUnpinned',
+  'columnHeader--siblingFocused',
   'columnHeaderCheckbox',
   'columnHeaderDraggableContainer',
   'columnHeaderTitle',
diff --git a/packages/x-data-grid/src/hooks/features/columnHeaders/useGridColumnHeaders.tsx b/packages/x-data-grid/src/hooks/features/columnHeaders/useGridColumnHeaders.tsx
index 1b8d2a88a567c..c6bb0d81a9e6b 100644
--- a/packages/x-data-grid/src/hooks/features/columnHeaders/useGridColumnHeaders.tsx
+++ b/packages/x-data-grid/src/hooks/features/columnHeaders/useGridColumnHeaders.tsx
@@ -274,6 +274,17 @@ export const useGridColumnHeaders = (props: UseGridColumnHeadersProps) => {
         computedWidth: colDef.computedWidth,
       });
 
+      const siblingWithBorderingSeparator =
+        pinnedPosition === GridPinnedColumnPosition.RIGHT
+          ? renderedColumns[i - 1]
+          : renderedColumns[i + 1];
+      const isSiblingFocused = siblingWithBorderingSeparator
+        ? columnHeaderFocus !== null &&
+          columnHeaderFocus.field === siblingWithBorderingSeparator.field
+        : false;
+      const isLastUnpinned =
+        columnIndex + 1 === columnPositions.length - pinnedColumns.right.length;
+
       columns.push(
         <GridColumnHeaderItem
           key={colDef.field}
@@ -295,6 +306,8 @@ export const useGridColumnHeaders = (props: UseGridColumnHeadersProps) => {
           indexInSection={i}
           sectionLength={renderedColumns.length}
           gridHasFiller={gridHasFiller}
+          isLastUnpinned={isLastUnpinned}
+          isSiblingFocused={isSiblingFocused}
           {...other}
         />,
       );