diff --git a/keyserver/storage/postgres/device_keys_table.go b/keyserver/storage/postgres/device_keys_table.go
index af2641cce..e1b4e9475 100644
--- a/keyserver/storage/postgres/device_keys_table.go
+++ b/keyserver/storage/postgres/device_keys_table.go
@@ -102,8 +102,16 @@ func (s *deviceKeysStatements) SelectDeviceKeysJSON(ctx context.Context, keys []
 	return nil
 }
 
-func (s *deviceKeysStatements) SelectMaxStreamIDForUser(ctx context.Context, txn *sql.Tx, userID string) (streamID int, err error) {
-	err = txn.Stmt(s.selectMaxStreamForUserStmt).QueryRowContext(ctx, userID).Scan(&streamID)
+func (s *deviceKeysStatements) SelectMaxStreamIDForUser(ctx context.Context, txn *sql.Tx, userID string) (streamID int32, err error) {
+	// nullable if there are no results
+	var nullStream sql.NullInt32
+	err = txn.Stmt(s.selectMaxStreamForUserStmt).QueryRowContext(ctx, userID).Scan(&nullStream)
+	if err == sql.ErrNoRows {
+		err = nil
+	}
+	if nullStream.Valid {
+		streamID = nullStream.Int32
+	}
 	return
 }
 
diff --git a/keyserver/storage/shared/storage.go b/keyserver/storage/shared/storage.go
index 53d16f96c..e78ee9433 100644
--- a/keyserver/storage/shared/storage.go
+++ b/keyserver/storage/shared/storage.go
@@ -59,7 +59,7 @@ func (d *Database) StoreDeviceKeys(ctx context.Context, keys []api.DeviceMessage
 			if err != nil {
 				return err
 			}
-			userIDToStreamID[userID] = streamID
+			userIDToStreamID[userID] = int(streamID)
 		}
 		// set the stream IDs for each key
 		for i := range keys {
diff --git a/keyserver/storage/sqlite3/device_keys_table.go b/keyserver/storage/sqlite3/device_keys_table.go
index dd7cf9faa..9f70885ad 100644
--- a/keyserver/storage/sqlite3/device_keys_table.go
+++ b/keyserver/storage/sqlite3/device_keys_table.go
@@ -127,8 +127,16 @@ func (s *deviceKeysStatements) SelectDeviceKeysJSON(ctx context.Context, keys []
 	return nil
 }
 
-func (s *deviceKeysStatements) SelectMaxStreamIDForUser(ctx context.Context, txn *sql.Tx, userID string) (streamID int, err error) {
-	err = txn.Stmt(s.selectMaxStreamForUserStmt).QueryRowContext(ctx, userID).Scan(&streamID)
+func (s *deviceKeysStatements) SelectMaxStreamIDForUser(ctx context.Context, txn *sql.Tx, userID string) (streamID int32, err error) {
+	// nullable if there are no results
+	var nullStream sql.NullInt32
+	err = txn.Stmt(s.selectMaxStreamForUserStmt).QueryRowContext(ctx, userID).Scan(&nullStream)
+	if err == sql.ErrNoRows {
+		err = nil
+	}
+	if nullStream.Valid {
+		streamID = nullStream.Int32
+	}
 	return
 }
 
diff --git a/keyserver/storage/storage_test.go b/keyserver/storage/storage_test.go
index 66f6930f9..b3e45e6cc 100644
--- a/keyserver/storage/storage_test.go
+++ b/keyserver/storage/storage_test.go
@@ -6,6 +6,7 @@ import (
 	"testing"
 
 	"github.com/Shopify/sarama"
+	"github.com/matrix-org/dendrite/keyserver/api"
 )
 
 var ctx = context.Background()
@@ -77,3 +78,84 @@ func TestKeyChangesUpperLimit(t *testing.T) {
 		t.Fatalf("KeyChanges: wrong user_ids: %v", userIDs)
 	}
 }
+
+// The purpose of this test is to make sure that the storage layer is generating sequential stream IDs per user,
+// and that they are returned correctly when querying for device keys.
+func TestDeviceKeysStreamIDGeneration(t *testing.T) {
+	db, err := NewDatabase("file::memory:", nil)
+	if err != nil {
+		t.Fatalf("Failed to NewDatabase: %s", err)
+	}
+	alice := "@alice:TestDeviceKeysStreamIDGeneration"
+	bob := "@bob:TestDeviceKeysStreamIDGeneration"
+	msgs := []api.DeviceMessage{
+		{
+			DeviceKeys: api.DeviceKeys{
+				DeviceID: "AAA",
+				UserID:   alice,
+				KeyJSON:  []byte(`{"key":"v1"}`),
+			},
+			// StreamID: 1
+		},
+		{
+			DeviceKeys: api.DeviceKeys{
+				DeviceID: "AAA",
+				UserID:   bob,
+				KeyJSON:  []byte(`{"key":"v1"}`),
+			},
+			// StreamID: 1 as this is a different user
+		},
+		{
+			DeviceKeys: api.DeviceKeys{
+				DeviceID: "another_device",
+				UserID:   alice,
+				KeyJSON:  []byte(`{"key":"v1"}`),
+			},
+			// StreamID: 2 as this is a 2nd device key
+		},
+	}
+	MustNotError(t, db.StoreDeviceKeys(ctx, msgs))
+	if msgs[0].StreamID != 1 {
+		t.Fatalf("Expected StoreDeviceKeys to set StreamID=1 but got %d", msgs[0].StreamID)
+	}
+	if msgs[1].StreamID != 1 {
+		t.Fatalf("Expected StoreDeviceKeys to set StreamID=1 (different user) but got %d", msgs[1].StreamID)
+	}
+	if msgs[2].StreamID != 2 {
+		t.Fatalf("Expected StoreDeviceKeys to set StreamID=2 (another device) but got %d", msgs[2].StreamID)
+	}
+
+	// updating a device sets the next stream ID for that user
+	msgs = []api.DeviceMessage{
+		{
+			DeviceKeys: api.DeviceKeys{
+				DeviceID: "AAA",
+				UserID:   alice,
+				KeyJSON:  []byte(`{"key":"v2"}`),
+			},
+			// StreamID: 3
+		},
+	}
+	MustNotError(t, db.StoreDeviceKeys(ctx, msgs))
+	if msgs[0].StreamID != 3 {
+		t.Fatalf("Expected StoreDeviceKeys to set StreamID=3 (new key same device) but got %d", msgs[0].StreamID)
+	}
+
+	// Querying for device keys returns the latest stream IDs
+	msgs, err = db.DeviceKeysForUser(ctx, alice, []string{"AAA", "another_device"})
+	if err != nil {
+		t.Fatalf("DeviceKeysForUser returned error: %s", err)
+	}
+	wantStreamIDs := map[string]int{
+		"AAA":            3,
+		"another_device": 2,
+	}
+	if len(msgs) != len(wantStreamIDs) {
+		t.Fatalf("DeviceKeysForUser: wrong number of devices, got %d want %d", len(msgs), len(wantStreamIDs))
+	}
+	for _, m := range msgs {
+		if m.StreamID != wantStreamIDs[m.DeviceID] {
+			t.Errorf("DeviceKeysForUser: wrong returned stream ID for key, got %d want %d", m.StreamID, wantStreamIDs[m.DeviceID])
+		}
+	}
+}
diff --git a/keyserver/storage/tables/interface.go b/keyserver/storage/tables/interface.go
index d7c06a764..65da3310c 100644
--- a/keyserver/storage/tables/interface.go
+++ b/keyserver/storage/tables/interface.go
@@ -34,7 +34,7 @@ type OneTimeKeys interface {
 type DeviceKeys interface {
 	SelectDeviceKeysJSON(ctx context.Context, keys []api.DeviceMessage) error
 	InsertDeviceKeys(ctx context.Context, txn *sql.Tx, keys []api.DeviceMessage) error
-	SelectMaxStreamIDForUser(ctx context.Context, txn *sql.Tx, userID string) (streamID int, err error)
+	SelectMaxStreamIDForUser(ctx context.Context, txn *sql.Tx, userID string) (streamID int32, err error)
 	SelectBatchDeviceKeys(ctx context.Context, userID string, deviceIDs []string) ([]api.DeviceMessage, error)
 }