diff --git a/github/github.go b/github/github.go
index b9a2488aaf5..6de7174b925 100644
--- a/github/github.go
+++ b/github/github.go
@@ -723,9 +723,8 @@ func (e *Error) Error() string {
 // CheckResponse checks the API response for errors, and returns them if
 // present. A response is considered an error if it has a status code outside
 // the 200 range or equal to 202 Accepted.
-// API error responses are expected to have either no response
-// body, or a JSON response body that maps to ErrorResponse. Any other
-// response body will be silently ignored.
+// API error responses are expected to have response
+// body, and a JSON response body that maps to ErrorResponse.
 //
 // The error type will be *RateLimitError for rate limit exceeded errors,
 // *AcceptedError for 202 Accepted status codes,
@@ -742,6 +741,10 @@ func CheckResponse(r *http.Response) error {
 	if err == nil && data != nil {
 		json.Unmarshal(data, errorResponse)
 	}
+	// Re-populate error response body because GitHub error responses are often
+	// undocumented and inconsistent.
+	// Issue #1136, #540.
+	r.Body = ioutil.NopCloser(bytes.NewBuffer(data))
 	switch {
 	case r.StatusCode == http.StatusUnauthorized && strings.HasPrefix(r.Header.Get(headerOTP), "required"):
 		return (*TwoFactorAuthError)(errorResponse)
diff --git a/github/github_test.go b/github/github_test.go
index 1aa3ef9b1bb..2bde0ac3b5d 100644
--- a/github/github_test.go
+++ b/github/github_test.go
@@ -942,6 +942,36 @@ func TestCheckResponse_noBody(t *testing.T) {
 	}
 }
 
+func TestCheckResponse_unexpectedErrorStructure(t *testing.T) {
+	httpBody := `{"message":"m", "errors": ["error 1"]}`
+	res := &http.Response{
+		Request:    &http.Request{},
+		StatusCode: http.StatusBadRequest,
+		Body:       ioutil.NopCloser(strings.NewReader(httpBody)),
+	}
+	err := CheckResponse(res).(*ErrorResponse)
+
+	if err == nil {
+		t.Errorf("Expected error response.")
+	}
+
+	want := &ErrorResponse{
+		Response: res,
+		Message:  "m",
+		Errors:   []Error{{}},
+	}
+	if !reflect.DeepEqual(err, want) {
+		t.Errorf("Error = %#v, want %#v", err, want)
+	}
+	data, err2 := ioutil.ReadAll(err.Response.Body)
+	if err2 != nil {
+		t.Fatalf("failed to read response body: %v", err)
+	}
+	if got := string(data); got != httpBody {
+		t.Errorf("ErrorResponse.Response.Body = %q, want %q", got, httpBody)
+	}
+}
+
 func TestParseBooleanResponse_true(t *testing.T) {
 	result, err := parseBoolResponse(nil)
 	if err != nil {