diff --git a/src/material/sidenav/drawer.scss b/src/material/sidenav/drawer.scss
index f7e89895a873..8f2fbc08beea 100644
--- a/src/material/sidenav/drawer.scss
+++ b/src/material/sidenav/drawer.scss
@@ -109,6 +109,10 @@ $drawer-over-drawer-z-index: 4;
   height: 100%;
   overflow: auto;
 
+  &.mat-drawer-content-hidden {
+    opacity: 0;
+  }
+
   .mat-drawer-transition & {
     transition: {
       duration: variables.$swift-ease-out-duration;
diff --git a/src/material/sidenav/drawer.ts b/src/material/sidenav/drawer.ts
index b05af6537231..361440a53834 100644
--- a/src/material/sidenav/drawer.ts
+++ b/src/material/sidenav/drawer.ts
@@ -93,6 +93,7 @@ export function MAT_DRAWER_DEFAULT_AUTOSIZE_FACTORY(): boolean {
     'class': 'mat-drawer-content',
     '[style.margin-left.px]': '_container._contentMargins.left',
     '[style.margin-right.px]': '_container._contentMargins.right',
+    '[class.mat-drawer-content-hidden]': '_shouldBeHidden()',
   },
   changeDetection: ChangeDetectionStrategy.OnPush,
   encapsulation: ViewEncapsulation.None,
@@ -104,6 +105,7 @@ export function MAT_DRAWER_DEFAULT_AUTOSIZE_FACTORY(): boolean {
   ],
 })
 export class MatDrawerContent extends CdkScrollable implements AfterContentInit {
+  private _platform = inject(Platform);
   private _changeDetectorRef = inject(ChangeDetectorRef);
   _container = inject(MatDrawerContainer);
 
@@ -122,6 +124,24 @@ export class MatDrawerContent extends CdkScrollable implements AfterContentInit
       this._changeDetectorRef.markForCheck();
     });
   }
+
+  /** Determines whether the content element should be hidden from the user. */
+  protected _shouldBeHidden(): boolean {
+    // In some modes the content is pushed based on the width of the opened sidenavs, however on
+    // the server we can't measure the sidenav so the margin is always zero. This can cause the
+    // content to jump around when it's rendered on the server and hydrated on the client. We
+    // avoid it by hiding the content on the initial render and then showing it once the sidenav
+    // has been measured on the client.
+    if (this._platform.isBrowser) {
+      return false;
+    }
+
+    const {start, end} = this._container;
+    return (
+      (start != null && start.mode !== 'over' && start.opened) ||
+      (end != null && end.mode !== 'over' && end.opened)
+    );
+  }
 }
 
 /**
diff --git a/src/material/sidenav/sidenav.ts b/src/material/sidenav/sidenav.ts
index e7214532f921..3a877964d9c2 100644
--- a/src/material/sidenav/sidenav.ts
+++ b/src/material/sidenav/sidenav.ts
@@ -30,8 +30,6 @@ import {CdkScrollable} from '@angular/cdk/scrolling';
   template: '<ng-content></ng-content>',
   host: {
     'class': 'mat-drawer-content mat-sidenav-content',
-    '[style.margin-left.px]': '_container._contentMargins.left',
-    '[style.margin-right.px]': '_container._contentMargins.right',
   },
   changeDetection: ChangeDetectionStrategy.OnPush,
   encapsulation: ViewEncapsulation.None,
diff --git a/tools/public_api_guard/material/sidenav.md b/tools/public_api_guard/material/sidenav.md
index 062c2ddddf52..8878fd1f9684 100644
--- a/tools/public_api_guard/material/sidenav.md
+++ b/tools/public_api_guard/material/sidenav.md
@@ -136,6 +136,7 @@ export class MatDrawerContent extends CdkScrollable implements AfterContentInit
     _container: MatDrawerContainer;
     // (undocumented)
     ngAfterContentInit(): void;
+    protected _shouldBeHidden(): boolean;
     // (undocumented)
     static ɵcmp: i0.ɵɵComponentDeclaration<MatDrawerContent, "mat-drawer-content", never, {}, {}, never, ["*"], true, never>;
     // (undocumented)