diff --git a/core/src/components.d.ts b/core/src/components.d.ts
index 7721801eb60..5e47667392b 100644
--- a/core/src/components.d.ts
+++ b/core/src/components.d.ts
@@ -868,6 +868,10 @@ export namespace Components {
           * Get the element where the actual scrolling takes place. This element can be used to subscribe to `scroll` events or manually modify `scrollTop`. However, it's recommended to use the API provided by `ion-content`:  i.e. Using `ionScroll`, `ionScrollStart`, `ionScrollEnd` for scrolling events and `scrollToPoint()` to scroll the content into a certain point.
          */
         "getScrollElement": () => Promise<HTMLElement>;
+        /**
+          * Recalculate content dimensions. Called by overlays (e.g., popover) when sibling elements like headers or footers have finished rendering and their heights are available, ensuring accurate offset-top calculations.
+         */
+        "recalculateDimensions": () => Promise<void>;
         /**
           * Scroll by a specified X/Y distance in the component.
           * @param x The amount to scroll by on the horizontal axis.
diff --git a/core/src/components/content/content.tsx b/core/src/components/content/content.tsx
index 74e44c63597..361939f7c27 100644
--- a/core/src/components/content/content.tsx
+++ b/core/src/components/content/content.tsx
@@ -254,6 +254,17 @@ export class Content implements ComponentInterface {
     }
   }
 
+  /**
+   * Recalculate content dimensions. Called by overlays (e.g., popover) when
+   * sibling elements like headers or footers have finished rendering and their
+   * heights are available, ensuring accurate offset-top calculations.
+   * @internal
+   */
+  @Method()
+  async recalculateDimensions(): Promise<void> {
+    readTask(() => this.readDimensions());
+  }
+
   private readDimensions() {
     const page = getPageElement(this.el);
     const top = Math.max(this.el.offsetTop, 0);
diff --git a/core/src/components/popover/popover.tsx b/core/src/components/popover/popover.tsx
index 9b07ab2f275..af0e613297d 100644
--- a/core/src/components/popover/popover.tsx
+++ b/core/src/components/popover/popover.tsx
@@ -64,6 +64,7 @@ export class Popover implements ComponentInterface, PopoverInterface {
   private destroyTriggerInteraction?: () => void;
   private destroyKeyboardInteraction?: () => void;
   private destroyDismissInteraction?: () => void;
+  private headerResizeObserver?: ResizeObserver;
 
   private inline = false;
   private workingDelegate?: FrameworkDelegate;
@@ -361,6 +362,11 @@ export class Popover implements ComponentInterface, PopoverInterface {
     if (destroyTriggerInteraction) {
       destroyTriggerInteraction();
     }
+
+    if (this.headerResizeObserver) {
+      this.headerResizeObserver.disconnect();
+      this.headerResizeObserver = undefined;
+    }
   }
 
   componentWillLoad() {
@@ -491,6 +497,8 @@ export class Popover implements ComponentInterface, PopoverInterface {
       inline
     );
 
+    this.recalculateContentOnHeaderReady();
+
     if (!this.keyboardEvents) {
       this.configureKeyboardInteraction();
     }
@@ -540,6 +548,39 @@ export class Popover implements ComponentInterface, PopoverInterface {
     unlock();
   }
 
+  /**
+   * Watch the header for height changes and trigger content dimension
+   * recalculation when the header has a height > 0. This sets the offset-top
+   * of the content to the height of the header correctly.
+   */
+  private recalculateContentOnHeaderReady() {
+    const popoverContent = this.el.shadowRoot?.querySelector('.popover-content');
+    if (!popoverContent) {
+      return;
+    }
+
+    const contentContainer = this.usersElement || popoverContent;
+
+    const header = contentContainer.querySelector('ion-header') as HTMLElement | null;
+    const contentElements = contentContainer.querySelectorAll('ion-content');
+
+    if (!header || contentElements.length === 0) {
+      return;
+    }
+
+    this.headerResizeObserver = new ResizeObserver(async () => {
+      if (header.offsetHeight > 0) {
+        this.headerResizeObserver?.disconnect();
+        this.headerResizeObserver = undefined;
+        for (const contentEl of contentElements) {
+          await contentEl.recalculateDimensions();
+        }
+      }
+    });
+
+    this.headerResizeObserver.observe(header);
+  }
+
   /**
    * Dismiss the popover overlay after it has been presented.
    * This is a no-op if the overlay has not been presented yet. If you want