diff --git a/tsweb/jsonhandler.go b/tsweb/jsonhandler.go
index 56704da7c..3199138e6 100644
--- a/tsweb/jsonhandler.go
+++ b/tsweb/jsonhandler.go
@@ -58,6 +58,9 @@ func (fn JSONHandlerFunc) ServeHTTPReturn(w http.ResponseWriter, r *http.Request
 			// the client in this handler. We don't want the wrapping
 			// ReturnHandler to do it too.
 			err = werr.Err
+			if werr.Msg != "" {
+				err = fmt.Errorf("%s: %w", werr.Msg, err)
+			}
 		} else {
 			resp = &response{
 				Status: "error",
diff --git a/tsweb/tsweb.go b/tsweb/tsweb.go
index 1c8ff01bc..649abdfa0 100644
--- a/tsweb/tsweb.go
+++ b/tsweb/tsweb.go
@@ -236,8 +236,13 @@ func (h retHandler) ServeHTTP(w http.ResponseWriter, r *http.Request) {
 	case hErrOK:
 		// Handler asked us to send an error. Do so, if we haven't
 		// already sent a response.
+		msg.Err = hErr.Msg
 		if hErr.Err != nil {
-			msg.Err = hErr.Err.Error()
+			if msg.Err == "" {
+				msg.Err = hErr.Err.Error()
+			} else {
+				msg.Err = msg.Err + ": " + hErr.Err.Error()
+			}
 		}
 		if lw.code != 0 {
 			h.logf("[unexpected] handler returned HTTPError %v, but already sent a response with code %d", hErr, lw.code)
diff --git a/tsweb/tsweb_test.go b/tsweb/tsweb_test.go
index 6b4dcaf28..2e94ef752 100644
--- a/tsweb/tsweb_test.go
+++ b/tsweb/tsweb_test.go
@@ -122,7 +122,7 @@ func TestStdHandler(t *testing.T) {
 				Host:       "example.com",
 				Method:     "GET",
 				RequestURI: "/foo",
-				Err:        testErr.Error(),
+				Err:        "not found: " + testErr.Error(),
 				Code:       404,
 			},
 		},
@@ -139,6 +139,7 @@ func TestStdHandler(t *testing.T) {
 				Host:       "example.com",
 				Method:     "GET",
 				RequestURI: "/foo",
+				Err:        "not found",
 				Code:       404,
 			},
 		},
@@ -189,7 +190,7 @@ func TestStdHandler(t *testing.T) {
 				Host:       "example.com",
 				Method:     "GET",
 				RequestURI: "/foo",
-				Err:        testErr.Error(),
+				Err:        "not found: " + testErr.Error(),
 				Code:       200,
 			},
 		},