diff --git a/serverkeyapi/api/api.go b/serverkeyapi/api/api.go
index f108d437..a43f9c0a 100644
--- a/serverkeyapi/api/api.go
+++ b/serverkeyapi/api/api.go
@@ -4,6 +4,7 @@ import (
 	"context"
 	"errors"
 	"net/http"
+	"time"
 
 	"github.com/matrix-org/dendrite/internal/caching"
 	"github.com/matrix-org/gomatrixserverlib"
@@ -69,9 +70,12 @@ func (s *httpServerKeyInternalAPI) FetcherName() string {
 }
 
 func (s *httpServerKeyInternalAPI) StoreKeys(
-	ctx context.Context,
+	_ context.Context,
 	results map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult,
 ) error {
+	// Run in a background context - we don't want to stop this work just
+	// because the caller gives up waiting.
+	ctx := context.Background()
 	request := InputPublicKeysRequest{
 		Keys: make(map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult),
 	}
@@ -84,9 +88,12 @@ func (s *httpServerKeyInternalAPI) StoreKeys(
 }
 
 func (s *httpServerKeyInternalAPI) FetchKeys(
-	ctx context.Context,
+	_ context.Context,
 	requests map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.Timestamp,
 ) (map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult, error) {
+	// Run in a background context - we don't want to stop this work just
+	// because the caller gives up waiting.
+	ctx := context.Background()
 	result := make(map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult)
 	request := QueryPublicKeysRequest{
 		Requests: make(map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.Timestamp),
@@ -94,8 +101,12 @@ func (s *httpServerKeyInternalAPI) FetchKeys(
 	response := QueryPublicKeysResponse{
 		Results: make(map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult),
 	}
+	now := gomatrixserverlib.AsTimestamp(time.Now())
 	for req, ts := range requests {
 		if res, ok := s.immutableCache.GetServerKey(req); ok {
+			if now > res.ValidUntilTS && res.ExpiredTS == gomatrixserverlib.PublicKeyNotExpired {
+				continue
+			}
 			result[req] = res
 			continue
 		}
diff --git a/serverkeyapi/internal/api.go b/serverkeyapi/internal/api.go
index cbae59d9..c63b23f0 100644
--- a/serverkeyapi/internal/api.go
+++ b/serverkeyapi/internal/api.go
@@ -3,6 +3,7 @@ package internal
 import (
 	"context"
 	"fmt"
+	"time"
 
 	"github.com/matrix-org/dendrite/internal/caching"
 	"github.com/matrix-org/dendrite/serverkeyapi/api"
@@ -24,25 +25,35 @@ func (s *ServerKeyAPI) KeyRing() *gomatrixserverlib.KeyRing {
 }
 
 func (s *ServerKeyAPI) StoreKeys(
-	ctx context.Context,
+	_ context.Context,
 	results map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult,
 ) error {
+	// Run in a background context - we don't want to stop this work just
+	// because the caller gives up waiting.
+	ctx := context.Background()
 	// Store any keys that we were given in our database.
 	return s.OurKeyRing.KeyDatabase.StoreKeys(ctx, results)
 }
 
 func (s *ServerKeyAPI) FetchKeys(
-	ctx context.Context,
+	_ context.Context,
 	requests map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.Timestamp,
 ) (map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult, error) {
+	// Run in a background context - we don't want to stop this work just
+	// because the caller gives up waiting.
+	ctx := context.Background()
 	results := map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult{}
 	// First consult our local database and see if we have the requested
 	// keys. These might come from a cache, depending on the database
 	// implementation used.
+	now := gomatrixserverlib.AsTimestamp(time.Now())
 	if dbResults, err := s.OurKeyRing.KeyDatabase.FetchKeys(ctx, requests); err == nil {
 		// We successfully got some keys. Add them to the results and
 		// remove them from the request list.
 		for req, res := range dbResults {
+			if now > res.ValidUntilTS && res.ExpiredTS == gomatrixserverlib.PublicKeyNotExpired {
+				continue
+			}
 			results[req] = res
 			delete(requests, req)
 		}
@@ -61,6 +72,9 @@ func (s *ServerKeyAPI) FetchKeys(
 				results[req] = res
 				delete(requests, req)
 			}
+			if err = s.OurKeyRing.KeyDatabase.StoreKeys(ctx, fetcherResults); err != nil {
+				return nil, fmt.Errorf("server key API failed to store retrieved keys: %w", err)
+			}
 		}
 	}
 	// If we failed to fetch any keys then we should report an error.
diff --git a/serverkeyapi/internal/http.go b/serverkeyapi/internal/http.go
index 30327571..eef66b76 100644
--- a/serverkeyapi/internal/http.go
+++ b/serverkeyapi/internal/http.go
@@ -14,28 +14,16 @@ import (
 func (s *ServerKeyAPI) SetupHTTP(internalAPIMux *mux.Router) {
 	internalAPIMux.Handle(api.ServerKeyQueryPublicKeyPath,
 		internal.MakeInternalAPI("queryPublicKeys", func(req *http.Request) util.JSONResponse {
-			result := map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.PublicKeyLookupResult{}
 			request := api.QueryPublicKeysRequest{}
 			response := api.QueryPublicKeysResponse{}
 			if err := json.NewDecoder(req.Body).Decode(&request); err != nil {
 				return util.MessageResponse(http.StatusBadRequest, err.Error())
 			}
-			lookup := make(map[gomatrixserverlib.PublicKeyLookupRequest]gomatrixserverlib.Timestamp)
-			for req, timestamp := range request.Requests {
-				if res, ok := s.ImmutableCache.GetServerKey(req); ok {
-					result[req] = res
-					continue
-				}
-				lookup[req] = timestamp
-			}
-			keys, err := s.FetchKeys(req.Context(), lookup)
+			keys, err := s.FetchKeys(req.Context(), request.Requests)
 			if err != nil {
 				return util.ErrorResponse(err)
 			}
-			for req, res := range keys {
-				result[req] = res
-			}
-			response.Results = result
+			response.Results = keys
 			return util.JSONResponse{Code: http.StatusOK, JSON: &response}
 		}),
 	)