diff --git a/internal/httputil/http.go b/internal/httputil/http.go
index ba2cc0284..ee6370bd1 100644
--- a/internal/httputil/http.go
+++ b/internal/httputil/http.go
@@ -71,13 +71,13 @@ func PostJSON[reqtype, restype any, errtype error](
 		return err
 	}
 	if res.StatusCode != http.StatusOK {
-		var errorBody errtype
-		if msgerr := json.NewDecoder(res.Body).Decode(&errorBody); msgerr != nil {
-			return fmt.Errorf("internal API: %d from %s", res.StatusCode, apiURL)
+		errorBody := new(errtype)
+		if err = json.NewDecoder(res.Body).Decode(errorBody); err != nil {
+			return fmt.Errorf("HTTP %d from %s", res.StatusCode, apiURL)
 		}
-		return errorBody
+		return *errorBody
 	}
-	if err := json.NewDecoder(res.Body).Decode(response); err != nil {
+	if err = json.NewDecoder(res.Body).Decode(response); err != nil {
 		return fmt.Errorf("json.NewDecoder.Decode: %w", err)
 	}
 	return nil
diff --git a/internal/httputil/internalapi.go b/internal/httputil/internalapi.go
index 5dcc596cc..fea7ff188 100644
--- a/internal/httputil/internalapi.go
+++ b/internal/httputil/internalapi.go
@@ -17,12 +17,23 @@ package httputil
 import (
 	"context"
 	"encoding/json"
+	"fmt"
 	"net/http"
+	"reflect"
 
 	"github.com/matrix-org/util"
 	opentracing "github.com/opentracing/opentracing-go"
 )
 
+type InternalAPIError struct {
+	Type    string
+	Message string
+}
+
+func (e InternalAPIError) Error() string {
+	return fmt.Sprintf("internal API returned %q error: %s", e.Type, e.Message)
+}
+
 func MakeInternalRPCAPI[reqtype, restype any](metricsName string, f func(context.Context, *reqtype, *restype) error) http.Handler {
 	return MakeInternalAPI(metricsName, func(req *http.Request) util.JSONResponse {
 		var request reqtype
@@ -31,9 +42,18 @@ func MakeInternalRPCAPI[reqtype, restype any](metricsName string, f func(context
 			return util.MessageResponse(http.StatusBadRequest, err.Error())
 		}
 		if err := f(req.Context(), &request, &response); err != nil {
-			return util.ErrorResponse(err)
+			return util.JSONResponse{
+				Code: http.StatusInternalServerError,
+				JSON: &InternalAPIError{
+					Type:    reflect.TypeOf(err).String(),
+					Message: fmt.Sprintf("%s", err),
+				},
+			}
+		}
+		return util.JSONResponse{
+			Code: http.StatusOK,
+			JSON: &response,
 		}
-		return util.JSONResponse{Code: http.StatusOK, JSON: &response}
 	})
 }
 
@@ -45,9 +65,18 @@ func MakeInternalProxyAPI[reqtype, restype any](metricsName string, f func(conte
 		}
 		response, err := f(req.Context(), &request)
 		if err != nil {
-			return util.ErrorResponse(err)
+			return util.JSONResponse{
+				Code: http.StatusInternalServerError,
+				JSON: &InternalAPIError{
+					Type:    reflect.TypeOf(err).String(),
+					Message: fmt.Sprintf("%s", err),
+				},
+			}
+		}
+		return util.JSONResponse{
+			Code: http.StatusOK,
+			JSON: response,
 		}
-		return util.JSONResponse{Code: http.StatusOK, JSON: response}
 	})
 }
 
@@ -55,7 +84,7 @@ func CallInternalRPCAPI[req, res any](name, url string, client *http.Client, ctx
 	span, ctx := opentracing.StartSpanFromContext(ctx, name)
 	defer span.Finish()
 
-	return PostJSON[req, res, error](ctx, span, client, url, request, response)
+	return PostJSON[req, res, InternalAPIError](ctx, span, client, url, request, response)
 }
 
 func CallInternalProxyAPI[req, res any, errtype error](name, url string, client *http.Client, ctx context.Context, request *req) (res, error) {