diff --git a/docs/api-operation.md b/docs/api-operation.md
index 768697f91..c4a69cdce 100644
--- a/docs/api-operation.md
+++ b/docs/api-operation.md
@@ -18,6 +18,8 @@ The use of `rotate` without an angle will remove the EXIF `Orientation` tag, if
 Only one rotation can occur per pipeline.
 Previous calls to `rotate` in the same pipeline will be ignored.
 
+Multi-page images can only be rotated by 180 degrees.
+
 Method order is important when rotating, resizing and/or extracting regions,
 for example `.rotate(x).extract(y)` will produce a different result to `.extract(y).rotate(x)`.
 
diff --git a/docs/changelog.md b/docs/changelog.md
index 0e143bb63..a418d0803 100644
--- a/docs/changelog.md
+++ b/docs/changelog.md
@@ -13,6 +13,9 @@ Requires libvips v8.15.0
 * Ensure `extend` operation stays sequential when copying (regression in 0.32.0).
   [#3928](https://github.com/lovell/sharp/issues/3928)
 
+* Improve error handling for unsupported multi-page rotation.
+  [#3940](https://github.com/lovell/sharp/issues/3940)
+
 ### v0.33.1 - 17th December 2023
 
 * Add support for Yarn Plug'n'Play filesystem layout.
diff --git a/lib/operation.js b/lib/operation.js
index 199a0ebec..ed6df8345 100644
--- a/lib/operation.js
+++ b/lib/operation.js
@@ -24,6 +24,8 @@ const is = require('./is');
  * Only one rotation can occur per pipeline.
  * Previous calls to `rotate` in the same pipeline will be ignored.
  *
+ * Multi-page images can only be rotated by 180 degrees.
+ *
  * Method order is important when rotating, resizing and/or extracting regions,
  * for example `.rotate(x).extract(y)` will produce a different result to `.extract(y).rotate(x)`.
  *
diff --git a/src/pipeline.cc b/src/pipeline.cc
index 3e76cf8bf..791f208bc 100644
--- a/src/pipeline.cc
+++ b/src/pipeline.cc
@@ -96,6 +96,9 @@ class PipelineWorker : public Napi::AsyncWorker {
           baton->rotationAngle != 0.0);
 
         if (autoRotation != VIPS_ANGLE_D0) {
+          if (autoRotation != VIPS_ANGLE_D180) {
+            MultiPageUnsupported(nPages, "Rotate");
+          }
           image = image.rot(autoRotation);
           autoRotation = VIPS_ANGLE_D0;
         }
@@ -114,6 +117,9 @@ class PipelineWorker : public Napi::AsyncWorker {
           baton->flop = FALSE;
         }
         if (rotation != VIPS_ANGLE_D0) {
+          if (rotation != VIPS_ANGLE_D180) {
+            MultiPageUnsupported(nPages, "Rotate");
+          }
           image = image.rot(rotation);
           rotation = VIPS_ANGLE_D0;
         }
@@ -397,6 +403,9 @@ class PipelineWorker : public Napi::AsyncWorker {
         rotation != VIPS_ANGLE_D0);
       // Auto-rotate post-extract
       if (autoRotation != VIPS_ANGLE_D0) {
+        if (autoRotation != VIPS_ANGLE_D180) {
+          MultiPageUnsupported(nPages, "Rotate");
+        }
         image = image.rot(autoRotation);
       }
       // Mirror vertically (up-down) about the x-axis
@@ -409,6 +418,9 @@ class PipelineWorker : public Napi::AsyncWorker {
       }
       // Rotate post-extract 90-angle
       if (rotation != VIPS_ANGLE_D0) {
+        if (rotation != VIPS_ANGLE_D180) {
+          MultiPageUnsupported(nPages, "Rotate");
+        }
         image = image.rot(rotation);
       }
 
diff --git a/test/unit/rotate.js b/test/unit/rotate.js
index aee20eade..e9e819afe 100644
--- a/test/unit/rotate.js
+++ b/test/unit/rotate.js
@@ -353,6 +353,21 @@ describe('Rotation', function () {
     )
   );
 
+  it('Animated image rotate 180', () =>
+    assert.doesNotReject(() => sharp(fixtures.inputGifAnimated, { animated: true })
+      .rotate(180)
+      .toBuffer()
+    )
+  );
+
+  it('Animated image rotate non-180 rejects', () =>
+    assert.rejects(() => sharp(fixtures.inputGifAnimated, { animated: true })
+      .rotate(90)
+      .toBuffer(),
+    /Rotate is not supported for multi-page images/
+    )
+  );
+
   it('Multiple rotate emits warning', () => {
     let warningMessage = '';
     const s = sharp();