diff --git a/lib/interceptor/dns.js b/lib/interceptor/dns.js
index fc5dc1a4366..513a6e1f7df 100644
--- a/lib/interceptor/dns.js
+++ b/lib/interceptor/dns.js
@@ -349,7 +349,7 @@ module.exports = interceptorOpts => {
 
       instance.runLookup(origin, origDispatchOpts, (err, newOrigin) => {
         if (err) {
-          return handler.onError(err)
+          return handler.onResponseError(null, err)
         }
 
         let dispatchOpts = null
diff --git a/test/interceptors/dns.js b/test/interceptors/dns.js
index 944c190492e..436a81e6af2 100644
--- a/test/interceptors/dns.js
+++ b/test/interceptors/dns.js
@@ -1814,3 +1814,28 @@ test('#3937 - Handle host correctly', async t => {
   t.equal(response2.statusCode, 200)
   t.equal(await response2.body.text(), 'hello world!')
 })
+
+test('#3951 - Should handle lookup errors correctly', async t => {
+  const suite = tspl(t, { plan: 1 })
+
+  const requestOptions = {
+    method: 'GET',
+    path: '/',
+    headers: {
+      'content-type': 'application/json'
+    }
+  }
+
+  const client = new Agent().compose([
+    dns({
+      lookup: (_origin, _opts, cb) => {
+        cb(new Error('lookup error'))
+      }
+    })
+  ])
+
+  suite.rejects(client.request({
+    ...requestOptions,
+    origin: 'http://localhost'
+  }), new Error('lookup error'))
+})