diff --git a/roomserver/api/api.go b/roomserver/api/api.go
index 4ad308a3e..8e26854a1 100644
--- a/roomserver/api/api.go
+++ b/roomserver/api/api.go
@@ -2,6 +2,7 @@ package api
 
 import (
 	"context"
+	"crypto/ed25519"
 
 	"github.com/matrix-org/gomatrixserverlib"
 	"github.com/matrix-org/gomatrixserverlib/spec"
@@ -66,6 +67,9 @@ type RoomserverInternalAPI interface {
 		req *QueryAuthChainRequest,
 		res *QueryAuthChainResponse,
 	) error
+
+	// GetOrCreateUserRoomPrivateKey gets the user room key for the specified user. If no key exists yet, a new one is created.
+	GetOrCreateUserRoomPrivateKey(ctx context.Context, userID spec.UserID, roomID spec.RoomID) (ed25519.PrivateKey, error)
 }
 
 type InputRoomEventsAPI interface {
diff --git a/roomserver/internal/api.go b/roomserver/internal/api.go
index 1e5aba57c..7943ae5c0 100644
--- a/roomserver/internal/api.go
+++ b/roomserver/internal/api.go
@@ -2,6 +2,7 @@ package internal
 
 import (
 	"context"
+	"crypto/ed25519"
 
 	"github.com/getsentry/sentry-go"
 	"github.com/matrix-org/gomatrixserverlib"
@@ -271,3 +272,23 @@ func (r *RoomserverInternalAPI) PerformForget(
 ) error {
 	return r.Forgetter.PerformForget(ctx, req, resp)
 }
+
+// GetOrCreateUserRoomPrivateKey gets the user room key for the specified user. If no key exists yet, a new one is created.
+func (r *RoomserverInternalAPI) GetOrCreateUserRoomPrivateKey(ctx context.Context, userID spec.UserID, roomID spec.RoomID) (ed25519.PrivateKey, error) {
+	key, err := r.DB.SelectUserRoomPrivateKey(ctx, userID, roomID)
+	if err != nil {
+		return nil, err
+	}
+	// no key found, create one
+	if len(key) == 0 {
+		_, key, err = ed25519.GenerateKey(nil)
+		if err != nil {
+			return nil, err
+		}
+		key, err = r.DB.InsertUserRoomPrivatePublicKey(ctx, userID, roomID, key)
+		if err != nil {
+			return nil, err
+		}
+	}
+	return key, nil
+}
diff --git a/roomserver/internal/perform/perform_create_room.go b/roomserver/internal/perform/perform_create_room.go
index b81627b04..a79b369a4 100644
--- a/roomserver/internal/perform/perform_create_room.go
+++ b/roomserver/internal/perform/perform_create_room.go
@@ -353,7 +353,30 @@ func (c *Creator) PerformCreateRoom(ctx context.Context, userID spec.UserID, roo
 			SendAsServer: api.DoNotSendToOtherServers,
 		})
 	}
-	if err = api.SendInputRoomEvents(ctx, c.RSAPI, userID.Domain(), inputs, false); err != nil {
+
+	// first send the `m.room.create` event, so we have a roomNID
+	if err = api.SendInputRoomEvents(ctx, c.RSAPI, userID.Domain(), inputs[:1], false); err != nil {
+		util.GetLogger(ctx).WithError(err).Error("roomserverAPI.SendInputRoomEvents failed")
+		return "", &util.JSONResponse{
+			Code: http.StatusInternalServerError,
+			JSON: spec.InternalServerError{},
+		}
+	}
+
+	// create user room key if needed
+	if createRequest.RoomVersion == gomatrixserverlib.RoomVersionPseudoIDs {
+		_, err = c.RSAPI.GetOrCreateUserRoomPrivateKey(ctx, userID, roomID)
+		if err != nil {
+			util.GetLogger(ctx).WithError(err).Error("GetOrCreateUserRoomPrivateKey failed")
+			return "", &util.JSONResponse{
+				Code: http.StatusInternalServerError,
+				JSON: spec.InternalServerError{},
+			}
+		}
+	}
+
+	// send the remaining events
+	if err = api.SendInputRoomEvents(ctx, c.RSAPI, userID.Domain(), inputs[1:], false); err != nil {
 		util.GetLogger(ctx).WithError(err).Error("roomserverAPI.SendInputRoomEvents failed")
 		return "", &util.JSONResponse{
 			Code: http.StatusInternalServerError,
diff --git a/roomserver/internal/perform/perform_invite.go b/roomserver/internal/perform/perform_invite.go
index 8f188994f..babd5f812 100644
--- a/roomserver/internal/perform/perform_invite.go
+++ b/roomserver/internal/perform/perform_invite.go
@@ -188,6 +188,14 @@ func (r *Inviter) PerformInvite(
 		inviteEvent = event
 	}
 
+	// if we invited a local user, we can also create a user room key, if it doesn't exist yet.
+	if isTargetLocal && event.Version() == gomatrixserverlib.RoomVersionPseudoIDs {
+		_, err = r.RSAPI.GetOrCreateUserRoomPrivateKey(ctx, *invitedUser, *validRoomID)
+		if err != nil {
+			return fmt.Errorf("failed to get user room private key: %w", err)
+		}
+	}
+
 	// Send the invite event to the roomserver input stream. This will
 	// notify existing users in the room about the invite, update the
 	// membership table and ensure that the event is ready and available
diff --git a/roomserver/internal/perform/perform_join.go b/roomserver/internal/perform/perform_join.go
index ffabeabab..11d2bf395 100644
--- a/roomserver/internal/perform/perform_join.go
+++ b/roomserver/internal/perform/perform_join.go
@@ -308,6 +308,15 @@ func (r *Joiner) performJoinRoomByID(
 
 	switch err.(type) {
 	case nil:
+		// create user room key if needed
+		if buildRes.RoomVersion == gomatrixserverlib.RoomVersionPseudoIDs {
+			_, err = r.RSAPI.GetOrCreateUserRoomPrivateKey(ctx, *userID, *roomID)
+			if err != nil {
+				logrus.WithError(err).Error("GetOrCreateUserRoomPrivateKey failed")
+				return "", "", fmt.Errorf("failed to get user room private key: %w", err)
+			}
+		}
+
 		// The room join is local. Send the new join event into the
 		// roomserver. First of all check that the user isn't already
 		// a member of the room. This is best-effort (as in we won't
diff --git a/roomserver/storage/interface.go b/roomserver/storage/interface.go
index 447b90552..7156c11cc 100644
--- a/roomserver/storage/interface.go
+++ b/roomserver/storage/interface.go
@@ -31,6 +31,7 @@ type Database interface {
 	UserRoomKeys
 	// Do we support processing input events for more than one room at a time?
 	SupportsConcurrentRoomInputs() bool
+	AssignRoomNID(ctx context.Context, roomID spec.RoomID, roomVersion gomatrixserverlib.RoomVersion) (roomNID types.RoomNID, err error)
 	// RoomInfo returns room information for the given room ID, or nil if there is no room.
 	RoomInfo(ctx context.Context, roomID string) (*types.RoomInfo, error)
 	RoomInfoByNID(ctx context.Context, roomNID types.RoomNID) (*types.RoomInfo, error)
@@ -213,6 +214,7 @@ type UserRoomKeys interface {
 type RoomDatabase interface {
 	EventDatabase
 	UserRoomKeys
+	AssignRoomNID(ctx context.Context, roomID spec.RoomID, roomVersion gomatrixserverlib.RoomVersion) (roomNID types.RoomNID, err error)
 	// RoomInfo returns room information for the given room ID, or nil if there is no room.
 	RoomInfo(ctx context.Context, roomID string) (*types.RoomInfo, error)
 	RoomInfoByNID(ctx context.Context, roomNID types.RoomNID) (*types.RoomInfo, error)
diff --git a/roomserver/storage/shared/storage.go b/roomserver/storage/shared/storage.go
index 1cd0f23a2..61a3520a4 100644
--- a/roomserver/storage/shared/storage.go
+++ b/roomserver/storage/shared/storage.go
@@ -662,6 +662,26 @@ func (d *Database) IsEventRejected(ctx context.Context, roomNID types.RoomNID, e
 	return d.EventsTable.SelectEventRejected(ctx, nil, roomNID, eventID)
 }
 
+func (d *Database) AssignRoomNID(ctx context.Context, roomID spec.RoomID, roomVersion gomatrixserverlib.RoomVersion) (roomNID types.RoomNID, err error) {
+	// This should already be checked, let's check it anyway.
+	_, err = gomatrixserverlib.GetRoomVersion(roomVersion)
+	if err != nil {
+		return 0, err
+	}
+	err = d.Writer.Do(d.DB, nil, func(txn *sql.Tx) error {
+		roomNID, err = d.assignRoomNID(ctx, txn, roomID.String(), roomVersion)
+		if err != nil {
+			return err
+		}
+		return nil
+	})
+	if err != nil {
+		return 0, err
+	}
+	// Not setting caches, as assignRoomNID already does this
+	return roomNID, err
+}
+
 // GetOrCreateRoomInfo gets or creates a new RoomInfo, which is only safe to use with functions only needing a roomVersion or roomNID.
 func (d *Database) GetOrCreateRoomInfo(ctx context.Context, event gomatrixserverlib.PDU) (roomInfo *types.RoomInfo, err error) {
 	// Get the default room version. If the client doesn't supply a room_version
@@ -1692,7 +1712,7 @@ func (d *Database) SelectUserRoomPrivateKey(ctx context.Context, userID spec.Use
 			return rErr
 		}
 		if roomInfo == nil {
-			return nil
+			return eventutil.ErrRoomNoExists{}
 		}
 
 		key, sErr = d.UserRoomKeyTable.SelectUserRoomPrivateKey(ctx, txn, stateKeyNID, roomInfo.RoomNID)
diff --git a/roomserver/storage/shared/storage_test.go b/roomserver/storage/shared/storage_test.go
index 8f83af3bb..c7b915c7d 100644
--- a/roomserver/storage/shared/storage_test.go
+++ b/roomserver/storage/shared/storage_test.go
@@ -7,6 +7,7 @@ import (
 	"time"
 
 	"github.com/matrix-org/dendrite/internal/caching"
+	"github.com/matrix-org/dendrite/roomserver/types"
 	"github.com/matrix-org/gomatrixserverlib"
 	"github.com/matrix-org/gomatrixserverlib/spec"
 	"github.com/stretchr/testify/assert"
@@ -204,3 +205,24 @@ func TestUserRoomKeys(t *testing.T) {
 		assert.Error(t, err)
 	})
 }
+
+func TestAssignRoomNID(t *testing.T) {
+	ctx := context.Background()
+	alice := test.NewUser(t)
+	room := test.NewRoom(t, alice)
+
+	roomID, err := spec.NewRoomID(room.ID)
+	assert.NoError(t, err)
+
+	test.WithAllDatabases(t, func(t *testing.T, dbType test.DBType) {
+		db, close := mustCreateRoomserverDatabase(t, dbType)
+		defer close()
+
+		nid, err := db.AssignRoomNID(ctx, *roomID, room.Version)
+		assert.NoError(t, err)
+		assert.Greater(t, nid, types.EventNID(0))
+
+		_, err = db.AssignRoomNID(ctx, spec.RoomID{}, "notaroomversion")
+		assert.Error(t, err)
+	})
+}