diff --git a/src/components/feedback/Popover.tsx b/src/components/feedback/Popover.tsx
index e5814ec76..2e625af4c 100644
--- a/src/components/feedback/Popover.tsx
+++ b/src/components/feedback/Popover.tsx
@@ -133,9 +133,9 @@ function usePopoverPositioning(
 
     // First of all, open popover if it's using the native API, otherwise its
     // size is 0x0 and positioning calculations won't work.
-    const popover = popoverRef.current;
+    const popover = popoverRef.current!;
     if (asNativePopover) {
-      popover?.togglePopover(true);
+      popover.togglePopover(true);
     }
 
     const cleanup = adjustPopoverPositioning();
@@ -151,12 +151,18 @@ function usePopoverPositioning(
       capture: true,
     });
 
+    // Readjust popover positioning if its resized, in case it dropped-up, and
+    // it needs to be moved down
+    const observer = new ResizeObserver(adjustPopoverPositioning);
+    observer.observe(popover);
+
     return () => {
       if (asNativePopover) {
         popover?.togglePopover(false);
       }
       cleanup();
       listeners.removeAll();
+      observer.disconnect();
     };
   }, [adjustPopoverPositioning, asNativePopover, popoverOpen, popoverRef]);
 }
diff --git a/src/components/feedback/test/Popover-test.js b/src/components/feedback/test/Popover-test.js
index af8cd5d70..42ae05c88 100644
--- a/src/components/feedback/test/Popover-test.js
+++ b/src/components/feedback/test/Popover-test.js
@@ -1,4 +1,4 @@
-import { mount } from '@hypothesis/frontend-testing';
+import { mount, waitFor } from '@hypothesis/frontend-testing';
 import { useRef, useState } from 'preact/hooks';
 
 import Popover, { POPOVER_VIEWPORT_HORIZONTAL_GAP } from '../Popover';
@@ -73,6 +73,20 @@ describe('Popover', () => {
     return popoverTop < buttonTop;
   };
 
+  const getDistanceBetweenButtonAndPopover = wrapper => {
+    const appearedAbove = popoverAppearedAbove(wrapper);
+    const { top: popoverTop, bottom: popoverBottom } = getPopover(wrapper)
+      .getDOMNode()
+      .getBoundingClientRect();
+    const { top: buttonTop, bottom: buttonBottom } = getToggleButton(wrapper)
+      .getDOMNode()
+      .getBoundingClientRect();
+
+    return Math.abs(
+      appearedAbove ? popoverBottom - buttonTop : buttonBottom - popoverTop,
+    );
+  };
+
   [
     {
       restoreFocusOnClose: undefined, // Defaults to true
@@ -151,6 +165,42 @@ describe('Popover', () => {
     });
   });
 
+  [true, false].forEach(asNativePopover => {
+    it('repositions popover if it is resized after being open', async () => {
+      const wrapper = createComponent(
+        {
+          asNativePopover,
+          children: (
+            <>
+              <p>one</p>
+              <p>two</p>
+              <p>three</p>
+            </>
+          ),
+        },
+        { paddingTop: 1000 }, // Ensure popover appears above
+      );
+      togglePopover(wrapper);
+
+      // This applies only when the popover appears above, so let's verify it
+      assert.isTrue(popoverAppearedAbove(wrapper));
+
+      // After opening the popover, its distance to the button should be the
+      // same, even if it's resized
+      const distanceBeforeResizing =
+        getDistanceBetweenButtonAndPopover(wrapper);
+      wrapper.setProps({ children: 'Just one line' });
+
+      // Repositioning happens asynchronously via ResizeObserver, so we need to
+      // wait for it to eventually happen.
+      await waitFor(
+        () =>
+          distanceBeforeResizing ===
+          getDistanceBetweenButtonAndPopover(wrapper),
+      );
+    });
+  });
+
   context('when popover is supported', () => {
     [undefined, true].forEach(asNativePopover => {
       it('opens via popover API', async () => {