diff --git a/packages/grid/src/vaadin-grid-keyboard-navigation-mixin.js b/packages/grid/src/vaadin-grid-keyboard-navigation-mixin.js
index 4908a28eba..6d1d748569 100644
--- a/packages/grid/src/vaadin-grid-keyboard-navigation-mixin.js
+++ b/packages/grid/src/vaadin-grid-keyboard-navigation-mixin.js
@@ -751,6 +751,7 @@ export const KeyboardNavigationMixin = (superClass) =>
     _detectInteracting(e) {
       const isInteracting = e.composedPath().some((el) => el.localName === 'vaadin-grid-cell-content');
       this._setInteracting(isInteracting);
+      this.__updateHorizontalScrollPosition();
     }
 
     /** @private */
diff --git a/packages/grid/src/vaadin-grid-scroll-mixin.js b/packages/grid/src/vaadin-grid-scroll-mixin.js
index b02cb3b74f..5e15ae9a9a 100644
--- a/packages/grid/src/vaadin-grid-scroll-mixin.js
+++ b/packages/grid/src/vaadin-grid-scroll-mixin.js
@@ -245,26 +245,33 @@ export const ScrollMixin = (superClass) =>
     __updateHorizontalScrollPosition() {
       const scrollWidth = this.$.table.scrollWidth;
       const clientWidth = this.$.table.clientWidth;
-      const scrollLeft = this.__getNormalizedScrollLeft(this.$.table);
+      const scrollLeft = Math.max(0, this.$.table.scrollLeft);
+      const normalizedScrollLeft = this.__getNormalizedScrollLeft(this.$.table);
+
+      // Position header, footer and items container
+      const transform = `translate(${-scrollLeft}px, 0)`;
+      this.$.header.style.transform = transform;
+      this.$.footer.style.transform = transform;
+      this.$.items.style.transform = transform;
+
+      // Position frozen cells
+      const x = this.__isRTL ? normalizedScrollLeft + clientWidth - scrollWidth : scrollLeft;
+      const transformFrozen = `translate(${x}px, 0)`;
+      for (let i = 0; i < this._frozenCells.length; i++) {
+        this._frozenCells[i].style.transform = transformFrozen;
+      }
 
       // Position cells frozen to end
-      const remaining = scrollLeft + clientWidth - scrollWidth;
-
-      this.$.table.style.setProperty('--_grid-horizontal-scroll-remaining', remaining + 'px');
-      this.$.table.style.setProperty('--_grid-horizontal-scroll-position', -this._scrollLeft + 'px');
-
-      if (this.__isRTL) {
-        // Translating the sticky sections using a CSS variable works nicely on LTR.
-        // On RTL, it causes jumpy behavior (on Desktop Safari) so we need to translate manually.
-        const transformFrozen = `translate(${remaining}px, 0)`;
-        for (let i = 0; i < this._frozenCells.length; i++) {
-          this._frozenCells[i].style.transform = transformFrozen;
-        }
+      const remaining = this.__isRTL ? normalizedScrollLeft : scrollLeft + clientWidth - scrollWidth;
+      const transformFrozenToEnd = `translate(${remaining}px, 0)`;
+      for (let i = 0; i < this._frozenToEndCells.length; i++) {
+        this._frozenToEndCells[i].style.transform = transformFrozenToEnd;
+      }
 
-        const transformFrozenToEnd = `translate(${scrollLeft}px, 0)`;
-        for (let i = 0; i < this._frozenToEndCells.length; i++) {
-          this._frozenToEndCells[i].style.transform = transformFrozenToEnd;
-        }
+      // Only update the --_grid-horizontal-scroll-position custom property when navigating
+      // on row focus mode to avoid performance issues.
+      if (this.hasAttribute('navigating') && this.__rowFocusMode) {
+        this.$.table.style.setProperty('--_grid-horizontal-scroll-position', -x + 'px');
       }
     }
   };
diff --git a/packages/grid/src/vaadin-grid-styles.js b/packages/grid/src/vaadin-grid-styles.js
index 09b62d007b..7f019e7355 100644
--- a/packages/grid/src/vaadin-grid-styles.js
+++ b/packages/grid/src/vaadin-grid-styles.js
@@ -74,7 +74,6 @@ registerStyles(
 
     #header,
     #footer {
-      transform: translateX(var(--_grid-horizontal-scroll-position));
       display: block;
       position: -webkit-sticky;
       position: sticky;
@@ -102,7 +101,6 @@ registerStyles(
     }
 
     #items {
-      transform: translateX(var(--_grid-horizontal-scroll-position));
       flex-grow: 1;
       flex-shrink: 0;
       display: block;
@@ -164,15 +162,9 @@ registerStyles(
       display: none !important;
     }
 
-    [frozen] {
-      z-index: 2;
-      transform: translateX(calc(-1 * var(--_grid-horizontal-scroll-position)));
-      will-change: transform;
-    }
-
+    [frozen],
     [frozen-to-end] {
       z-index: 2;
-      transform: translateX(var(--_grid-horizontal-scroll-remaining));
       will-change: transform;
     }
 
@@ -293,10 +285,6 @@ registerStyles(
 
     /* RTL specific styles */
 
-    :host([dir='rtl']) *:is(#items, #header, #footer, [frozen], [frozen-to-end]) {
-      transform: none;
-    }
-
     :host([dir='rtl']) #items,
     :host([dir='rtl']) #header,
     :host([dir='rtl']) #footer {
diff --git a/packages/grid/test/keyboard-navigation.test.js b/packages/grid/test/keyboard-navigation.test.js
index 1a656b9047..bfc1341f89 100644
--- a/packages/grid/test/keyboard-navigation.test.js
+++ b/packages/grid/test/keyboard-navigation.test.js
@@ -5,6 +5,7 @@ import {
   fixtureSync,
   focusin,
   isChrome,
+  isDesktopSafari,
   keyboardEventFor,
   keyDownOn,
   keyUpOn,
@@ -1063,6 +1064,13 @@ describe('keyboard navigation', () => {
 
         flushGrid(grid);
 
+        // Force reflow to workaround a Safari rendering issue
+        if (isDesktopSafari) {
+          grid.style.display = 'flex';
+          await nextFrame();
+          grid.style.display = '';
+        }
+
         expect(grid.$.table.scrollLeft).to.equal(grid.$.table.scrollWidth - grid.$.table.offsetWidth);
       });