diff --git a/appservice/consumers/roomserver.go b/appservice/consumers/roomserver.go
index 9d723bed1..01790722a 100644
--- a/appservice/consumers/roomserver.go
+++ b/appservice/consumers/roomserver.go
@@ -56,7 +56,7 @@ func NewOutputRoomEventConsumer(
 		ctx:          process.Context(),
 		jetstream:    js,
 		durable:      cfg.Global.JetStream.Durable("AppserviceRoomserverConsumer"),
-		topic:        cfg.Global.JetStream.TopicFor(jetstream.OutputRoomEvent),
+		topic:        cfg.Global.JetStream.Prefixed(jetstream.OutputRoomEvent),
 		asDB:         appserviceDB,
 		rsAPI:        rsAPI,
 		serverName:   string(cfg.Global.ServerName),
diff --git a/clientapi/clientapi.go b/clientapi/clientapi.go
index 75184d3b7..4550343c7 100644
--- a/clientapi/clientapi.go
+++ b/clientapi/clientapi.go
@@ -55,7 +55,7 @@ func AddPublicRoutes(
 
 	syncProducer := &producers.SyncAPIProducer{
 		JetStream: js,
-		Topic:     cfg.Matrix.JetStream.TopicFor(jetstream.OutputClientData),
+		Topic:     cfg.Matrix.JetStream.Prefixed(jetstream.OutputClientData),
 	}
 
 	routing.Setup(
diff --git a/eduserver/eduserver.go b/eduserver/eduserver.go
index 9fe8704cf..91208a400 100644
--- a/eduserver/eduserver.go
+++ b/eduserver/eduserver.go
@@ -48,9 +48,9 @@ func NewInternalAPI(
 		Cache:                        eduCache,
 		UserAPI:                      userAPI,
 		JetStream:                    js,
-		OutputTypingEventTopic:       cfg.Matrix.JetStream.TopicFor(jetstream.OutputTypingEvent),
-		OutputSendToDeviceEventTopic: cfg.Matrix.JetStream.TopicFor(jetstream.OutputSendToDeviceEvent),
-		OutputReceiptEventTopic:      cfg.Matrix.JetStream.TopicFor(jetstream.OutputReceiptEvent),
+		OutputTypingEventTopic:       cfg.Matrix.JetStream.Prefixed(jetstream.OutputTypingEvent),
+		OutputSendToDeviceEventTopic: cfg.Matrix.JetStream.Prefixed(jetstream.OutputSendToDeviceEvent),
+		OutputReceiptEventTopic:      cfg.Matrix.JetStream.Prefixed(jetstream.OutputReceiptEvent),
 		ServerName:                   cfg.Matrix.ServerName,
 	}
 }
diff --git a/federationapi/consumers/eduserver.go b/federationapi/consumers/eduserver.go
index 1f81fa258..e14e60f47 100644
--- a/federationapi/consumers/eduserver.go
+++ b/federationapi/consumers/eduserver.go
@@ -58,9 +58,9 @@ func NewOutputEDUConsumer(
 		db:                store,
 		ServerName:        cfg.Matrix.ServerName,
 		durable:           cfg.Matrix.JetStream.Durable("FederationAPIEDUServerConsumer"),
-		typingTopic:       cfg.Matrix.JetStream.TopicFor(jetstream.OutputTypingEvent),
-		sendToDeviceTopic: cfg.Matrix.JetStream.TopicFor(jetstream.OutputSendToDeviceEvent),
-		receiptTopic:      cfg.Matrix.JetStream.TopicFor(jetstream.OutputReceiptEvent),
+		typingTopic:       cfg.Matrix.JetStream.Prefixed(jetstream.OutputTypingEvent),
+		sendToDeviceTopic: cfg.Matrix.JetStream.Prefixed(jetstream.OutputSendToDeviceEvent),
+		receiptTopic:      cfg.Matrix.JetStream.Prefixed(jetstream.OutputReceiptEvent),
 	}
 }
 
diff --git a/federationapi/consumers/keychange.go b/federationapi/consumers/keychange.go
index 33d716d25..94e454359 100644
--- a/federationapi/consumers/keychange.go
+++ b/federationapi/consumers/keychange.go
@@ -55,8 +55,8 @@ func NewKeyChangeConsumer(
 	return &KeyChangeConsumer{
 		ctx:        process.Context(),
 		jetstream:  js,
-		durable:    cfg.Matrix.JetStream.TopicFor("FederationAPIKeyChangeConsumer"),
-		topic:      cfg.Matrix.JetStream.TopicFor(jetstream.OutputKeyChangeEvent),
+		durable:    cfg.Matrix.JetStream.Prefixed("FederationAPIKeyChangeConsumer"),
+		topic:      cfg.Matrix.JetStream.Prefixed(jetstream.OutputKeyChangeEvent),
 		queues:     queues,
 		db:         store,
 		serverName: cfg.Matrix.ServerName,
diff --git a/federationapi/consumers/roomserver.go b/federationapi/consumers/roomserver.go
index 989f7cf49..ff2c8e5d4 100644
--- a/federationapi/consumers/roomserver.go
+++ b/federationapi/consumers/roomserver.go
@@ -61,7 +61,7 @@ func NewOutputRoomEventConsumer(
 		queues:    queues,
 		rsAPI:     rsAPI,
 		durable:   cfg.Matrix.JetStream.Durable("FederationAPIRoomServerConsumer"),
-		topic:     cfg.Matrix.JetStream.TopicFor(jetstream.OutputRoomEvent),
+		topic:     cfg.Matrix.JetStream.Prefixed(jetstream.OutputRoomEvent),
 	}
 }
 
diff --git a/keyserver/keyserver.go b/keyserver/keyserver.go
index cf66bd387..c557dfbaa 100644
--- a/keyserver/keyserver.go
+++ b/keyserver/keyserver.go
@@ -46,7 +46,7 @@ func NewInternalAPI(
 		logrus.WithError(err).Panicf("failed to connect to key server database")
 	}
 	keyChangeProducer := &producers.KeyChange{
-		Topic:     string(cfg.Matrix.JetStream.TopicFor(jetstream.OutputKeyChangeEvent)),
+		Topic:     string(cfg.Matrix.JetStream.Prefixed(jetstream.OutputKeyChangeEvent)),
 		JetStream: js,
 		DB:        db,
 	}
diff --git a/roomserver/internal/api.go b/roomserver/internal/api.go
index 91001e418..f96cefcb3 100644
--- a/roomserver/internal/api.go
+++ b/roomserver/internal/api.go
@@ -90,6 +90,7 @@ func (r *RoomserverInternalAPI) SetFederationAPI(fsAPI fsAPI.FederationInternalA
 	r.KeyRing = keyRing
 
 	r.Inputer = &input.Inputer{
+		Cfg:                  r.Cfg,
 		ProcessContext:       r.ProcessContext,
 		DB:                   r.DB,
 		InputRoomEventTopic:  r.InputRoomEventTopic,
diff --git a/roomserver/internal/input/input.go b/roomserver/internal/input/input.go
index c6e354611..6a8ae6d00 100644
--- a/roomserver/internal/input/input.go
+++ b/roomserver/internal/input/input.go
@@ -19,6 +19,7 @@ import (
 	"context"
 	"encoding/json"
 	"errors"
+	"fmt"
 	"sync"
 	"time"
 
@@ -29,6 +30,7 @@ import (
 	"github.com/matrix-org/dendrite/roomserver/api"
 	"github.com/matrix-org/dendrite/roomserver/internal/query"
 	"github.com/matrix-org/dendrite/roomserver/storage"
+	"github.com/matrix-org/dendrite/setup/config"
 	"github.com/matrix-org/dendrite/setup/jetstream"
 	"github.com/matrix-org/dendrite/setup/process"
 	"github.com/matrix-org/gomatrixserverlib"
@@ -45,7 +47,35 @@ var keyContentFields = map[string]string{
 	"m.room.member":             "membership",
 }
 
+// Inputer is responsible for consuming from the roomserver input
+// streams and processing the events. All input events are queued
+// into a single NATS stream and the order is preserved strictly.
+// The `room_id` message header will contain the room ID which will
+// be used to assign the pending event to a per-room worker.
+//
+// The input API maintains an ephemeral headers-only consumer. It
+// will speed through the stream working out which room IDs are
+// pending and create durable consumers for them. The durable
+// consumer will then be used for each room worker goroutine to
+// fetch events one by one and process them. Each room having a
+// durable consumer of its own means there is no head-of-line
+// blocking between rooms. Filtering ensures that each durable
+// consumer only receives events for the room it is interested in.
+//
+// The ephemeral consumer closely tracks the newest events. The
+// per-room durable consumers will only progress through the stream
+// as events are processed.
+//
+//       A BC *  -> positions of each consumer (* = ephemeral)
+//       ⌄ ⌄⌄ ⌄
+// ABAABCAABCAA  -> newest (letter = subject for each message)
+//
+// In this example, A is still processing an event but has two
+// pending events to process afterwards. Both B and C are caught
+// up, so they will do nothing until a new event comes in for B
+// or C.
 type Inputer struct {
+	Cfg                  *config.RoomServer
 	ProcessContext       *process.ProcessContext
 	DB                   storage.Database
 	NATSClient           *nats.Conn
@@ -57,147 +87,275 @@ type Inputer struct {
 	ACLs                 *acls.ServerACLs
 	InputRoomEventTopic  string
 	OutputRoomEventTopic string
-	workers              sync.Map // room ID -> *phony.Inbox
+	workers              sync.Map // room ID -> *worker
 
 	Queryer *query.Queryer
 }
 
-func (r *Inputer) workerForRoom(roomID string) *phony.Inbox {
-	inbox, _ := r.workers.LoadOrStore(roomID, &phony.Inbox{})
-	return inbox.(*phony.Inbox)
+type worker struct {
+	phony.Inbox
+	sync.Mutex
+	r            *Inputer
+	roomID       string
+	subscription *nats.Subscription
 }
 
-// eventsInProgress is an in-memory map to keep a track of which events we have
-// queued up for processing. If we get a redelivery from NATS and we still have
-// the queued up item then we won't do anything with the redelivered message. If
-// we've restarted Dendrite and now this map is empty then it means that we will
-// reload pending work from NATS.
-var eventsInProgress sync.Map
+func (r *Inputer) startWorkerForRoom(roomID string) {
+	v, loaded := r.workers.LoadOrStore(roomID, &worker{
+		r:      r,
+		roomID: roomID,
+	})
+	w := v.(*worker)
+	w.Lock()
+	defer w.Unlock()
+	if !loaded || w.subscription == nil {
+		consumer := r.Cfg.Matrix.JetStream.Prefixed("RoomInput" + jetstream.Tokenise(w.roomID))
+		subject := r.Cfg.Matrix.JetStream.Prefixed(jetstream.InputRoomEventSubj(w.roomID))
 
-// onMessage is called when a new event arrives in the roomserver input stream.
+		// Create the consumer. We do this as a specific step rather than
+		// letting PullSubscribe create it for us because we need the consumer
+		// to outlive the subscription. If we do it this way, we can Bind in the
+		// next step, and when we Unsubscribe, the consumer continues to live. If
+		// we leave PullSubscribe to create the durable consumer, Unsubscribe will
+		// delete it because it thinks it "owns" it, which in turn breaks the
+		// interest-based retention storage policy.
+		// If the durable consumer already exists, this is effectively a no-op.
+		// Another interesting tid-bit here: the ACK policy is set to "all" so that
+		// if we acknowledge a message, we also acknowledge everything that comes
+		// before it. This is necessary because otherwise our consumer will never
+		// acknowledge things we filtered out for other subjects and therefore they
+		// will linger around forever.
+		if _, err := w.r.JetStream.AddConsumer(
+			r.Cfg.Matrix.JetStream.Prefixed(jetstream.InputRoomEvent),
+			&nats.ConsumerConfig{
+				Durable:       consumer,
+				AckPolicy:     nats.AckAllPolicy,
+				DeliverPolicy: nats.DeliverAllPolicy,
+				FilterSubject: subject,
+				AckWait:       MaximumMissingProcessingTime + (time.Second * 10),
+			},
+		); err != nil {
+			logrus.WithError(err).Errorf("Failed to create consumer for room %q", w.roomID)
+			return
+		}
+
+		// Bind to our durable consumer. We want to receive all messages waiting
+		// for this subject and we want to manually acknowledge them, so that we
+		// can ensure they are only cleaned up when we are done processing them.
+		sub, err := w.r.JetStream.PullSubscribe(
+			subject, consumer,
+			nats.ManualAck(),
+			nats.DeliverAll(),
+			nats.AckWait(MaximumMissingProcessingTime+(time.Second*10)),
+			nats.Bind(r.InputRoomEventTopic, consumer),
+		)
+		if err != nil {
+			logrus.WithError(err).Errorf("Failed to subscribe to stream for room %q", w.roomID)
+			return
+		}
+
+		// Go and start pulling messages off the queue.
+		w.subscription = sub
+		w.Act(nil, w._next)
+	}
+}
+
+// Start creates an ephemeral non-durable consumer on the roomserver
+// input topic. It is configured to deliver us headers only because we
+// don't actually care about the contents of the message at this point,
+// we only care about the `room_id` field. Once a message arrives, we
+// will look to see if we have a worker for that room which has its
+// own consumer. If we don't, we'll start one.
 func (r *Inputer) Start() error {
 	_, err := r.JetStream.Subscribe(
-		r.InputRoomEventTopic,
-		// We specifically don't use jetstream.WithJetStreamMessage here because we
-		// queue the task off to a room-specific queue and the ACK needs to be sent
-		// later, possibly with an error response to the inputter if synchronous.
-		func(msg *nats.Msg) {
-			roomID := msg.Header.Get("room_id")
-			var inputRoomEvent api.InputRoomEvent
-			if err := json.Unmarshal(msg.Data, &inputRoomEvent); err != nil {
-				_ = msg.Term()
-				return
-			}
-
-			_ = msg.InProgress()
-			index := roomID + "\000" + inputRoomEvent.Event.EventID()
-			if _, ok := eventsInProgress.LoadOrStore(index, struct{}{}); ok {
-				// We're already waiting to deal with this event, so there's no
-				// point in queuing it up again. We've notified NATS that we're
-				// working on the message still, so that will have deferred the
-				// redelivery by a bit.
-				return
-			}
-
-			roomserverInputBackpressure.With(prometheus.Labels{"room_id": roomID}).Inc()
-			r.workerForRoom(roomID).Act(nil, func() {
-				_ = msg.InProgress() // resets the acknowledgement wait timer
-				defer eventsInProgress.Delete(index)
-				defer roomserverInputBackpressure.With(prometheus.Labels{"room_id": roomID}).Dec()
-				var errString string
-				if err := r.processRoomEvent(r.ProcessContext.Context(), &inputRoomEvent); err != nil {
-					if !errors.Is(err, context.DeadlineExceeded) && !errors.Is(err, context.Canceled) {
-						sentry.CaptureException(err)
-					}
-					logrus.WithError(err).WithFields(logrus.Fields{
-						"room_id":  roomID,
-						"event_id": inputRoomEvent.Event.EventID(),
-						"type":     inputRoomEvent.Event.Type(),
-					}).Warn("Roomserver failed to process async event")
-					_ = msg.Term()
-					errString = err.Error()
-				} else {
-					_ = msg.Ack()
-				}
-				if replyTo := msg.Header.Get("sync"); replyTo != "" {
-					if err := r.NATSClient.Publish(replyTo, []byte(errString)); err != nil {
-						logrus.WithError(err).WithFields(logrus.Fields{
-							"room_id":  roomID,
-							"event_id": inputRoomEvent.Event.EventID(),
-							"type":     inputRoomEvent.Event.Type(),
-						}).Warn("Roomserver failed to respond for sync event")
-					}
-				}
-			})
+		"", // This is blank because we specified it in BindStream.
+		func(m *nats.Msg) {
+			roomID := m.Header.Get(jetstream.RoomID)
+			r.startWorkerForRoom(roomID)
+			_ = m.Ack()
 		},
-		// NATS wants to acknowledge automatically by default when the message is
-		// read from the stream, but we want to override that behaviour by making
-		// sure that we only acknowledge when we're happy we've done everything we
-		// can. This ensures we retry things when it makes sense to do so.
-		nats.ManualAck(),
-		// Use a durable named consumer.
-		r.Durable,
-		// If we've missed things in the stream, e.g. we restarted, then replay
-		// all of the queued messages that were waiting for us.
+		nats.HeadersOnly(),
 		nats.DeliverAll(),
-		// Ensure that NATS doesn't try to resend us something that wasn't done
-		// within the period of time that we might still be processing it.
-		nats.AckWait(MaximumMissingProcessingTime+(time.Second*10)),
-		// It is recommended to disable this for pull consumers as per the docs:
-		// https://docs.nats.io/nats-concepts/jetstream/consumers#note-about-push-and-pull-consumers
-		nats.MaxAckPending(-1),
+		nats.AckAll(),
+		nats.BindStream(r.InputRoomEventTopic),
 	)
 	return err
 }
 
+// _next is called by the worker for the room. It must only be called
+// by the actor embedded into the worker.
+func (w *worker) _next() {
+	// Look up what the next event is that's waiting to be processed.
+	ctx, cancel := context.WithTimeout(w.r.ProcessContext.Context(), time.Minute)
+	defer cancel()
+	msgs, err := w.subscription.Fetch(1, nats.Context(ctx))
+	switch err {
+	case nil:
+		// Make sure that once we're done here, we queue up another call
+		// to _next in the inbox.
+		defer w.Act(nil, w._next)
+
+		// If no error was reported, but we didn't get exactly one message,
+		// then skip over this and try again on the next iteration.
+		if len(msgs) != 1 {
+			return
+		}
+
+	case context.DeadlineExceeded:
+		// The context exceeded, so we've been waiting for more than a
+		// minute for activity in this room. At this point we will shut
+		// down the subscriber to free up resources. It'll get started
+		// again if new activity happens.
+		if err = w.subscription.Unsubscribe(); err != nil {
+			logrus.WithError(err).Errorf("Failed to unsubscribe to stream for room %q", w.roomID)
+		}
+		w.Lock()
+		w.subscription = nil
+		w.Unlock()
+		return
+
+	default:
+		// Something went wrong while trying to fetch the next event
+		// from the queue. In which case, we'll shut down the subscriber
+		// and wait to be notified about new room activity again. Maybe
+		// the problem will be corrected by then.
+		logrus.WithError(err).Errorf("Failed to get next stream message for room %q", w.roomID)
+		if err = w.subscription.Unsubscribe(); err != nil {
+			logrus.WithError(err).Errorf("Failed to unsubscribe to stream for room %q", w.roomID)
+		}
+		w.Lock()
+		w.subscription = nil
+		w.Unlock()
+		return
+	}
+
+	// Try to unmarshal the input room event. If the JSON unmarshalling
+	// fails then we'll terminate the message — this notifies NATS that
+	// we are done with the message and never want to see it again.
+	msg := msgs[0]
+	var inputRoomEvent api.InputRoomEvent
+	if err = json.Unmarshal(msg.Data, &inputRoomEvent); err != nil {
+		_ = msg.Term()
+		return
+	}
+
+	roomserverInputBackpressure.With(prometheus.Labels{"room_id": w.roomID}).Inc()
+	defer roomserverInputBackpressure.With(prometheus.Labels{"room_id": w.roomID}).Dec()
+
+	// Process the room event. If something goes wrong then we'll tell
+	// NATS to terminate the message. We'll store the error result as
+	// a string, because we might want to return that to the caller if
+	// it was a synchronous request.
+	var errString string
+	if err = w.r.processRoomEvent(w.r.ProcessContext.Context(), &inputRoomEvent); err != nil {
+		if !errors.Is(err, context.DeadlineExceeded) && !errors.Is(err, context.Canceled) {
+			sentry.CaptureException(err)
+		}
+		logrus.WithError(err).WithFields(logrus.Fields{
+			"room_id":  w.roomID,
+			"event_id": inputRoomEvent.Event.EventID(),
+			"type":     inputRoomEvent.Event.Type(),
+		}).Warn("Roomserver failed to process async event")
+		_ = msg.Term()
+		errString = err.Error()
+	} else {
+		_ = msg.Ack()
+	}
+
+	// If it was a synchronous input request then the "sync" field
+	// will be present in the message. That means that someone is
+	// waiting for a response. The temporary inbox name is present in
+	// that field, so send back the error string (if any). If there
+	// was no error then we'll return a blank message, which means
+	// that everything was OK.
+	if replyTo := msg.Header.Get("sync"); replyTo != "" {
+		if err = w.r.NATSClient.Publish(replyTo, []byte(errString)); err != nil {
+			logrus.WithError(err).WithFields(logrus.Fields{
+				"room_id":  w.roomID,
+				"event_id": inputRoomEvent.Event.EventID(),
+				"type":     inputRoomEvent.Event.Type(),
+			}).Warn("Roomserver failed to respond for sync event")
+		}
+	}
+}
+
+// queueInputRoomEvents queues events into the roomserver input
+// stream in NATS.
+func (r *Inputer) queueInputRoomEvents(
+	ctx context.Context,
+	request *api.InputRoomEventsRequest,
+) (replySub *nats.Subscription, err error) {
+	// If the request is synchronous then we need to create a
+	// temporary inbox to wait for responses on, and then create
+	// a subscription to it. If it's asynchronous then we won't
+	// bother, so these values will remain empty.
+	var replyTo string
+	if !request.Asynchronous {
+		replyTo = nats.NewInbox()
+		replySub, err = r.NATSClient.SubscribeSync(replyTo)
+		if err != nil {
+			return nil, fmt.Errorf("r.NATSClient.SubscribeSync: %w", err)
+		}
+		if replySub == nil {
+			// This shouldn't ever happen, but it doesn't hurt to check
+			// because we can potentially avoid a nil pointer panic later
+			// if it did for some reason.
+			return nil, fmt.Errorf("expected a subscription to the temporary inbox")
+		}
+	}
+
+	// For each event, marshal the input room event and then
+	// send it into the input queue.
+	for _, e := range request.InputRoomEvents {
+		roomID := e.Event.RoomID()
+		subj := r.Cfg.Matrix.JetStream.Prefixed(jetstream.InputRoomEventSubj(roomID))
+		msg := &nats.Msg{
+			Subject: subj,
+			Header:  nats.Header{},
+		}
+		msg.Header.Set("room_id", roomID)
+		if replyTo != "" {
+			msg.Header.Set("sync", replyTo)
+		}
+		msg.Data, err = json.Marshal(e)
+		if err != nil {
+			return nil, fmt.Errorf("json.Marshal: %w", err)
+		}
+		if _, err = r.JetStream.PublishMsg(msg, nats.Context(ctx)); err != nil {
+			logrus.WithError(err).WithFields(logrus.Fields{
+				"room_id":  roomID,
+				"event_id": e.Event.EventID(),
+				"subj":     subj,
+			}).Error("Roomserver failed to queue async event")
+			return nil, fmt.Errorf("r.JetStream.PublishMsg: %w", err)
+		}
+	}
+	return
+}
+
 // InputRoomEvents implements api.RoomserverInternalAPI
 func (r *Inputer) InputRoomEvents(
 	ctx context.Context,
 	request *api.InputRoomEventsRequest,
 	response *api.InputRoomEventsResponse,
 ) {
-	var replyTo string
-	var replySub *nats.Subscription
-	if !request.Asynchronous {
-		var err error
-		replyTo = nats.NewInbox()
-		replySub, err = r.NATSClient.SubscribeSync(replyTo)
-		if err != nil {
-			response.ErrMsg = err.Error()
-			return
-		}
-	}
-
-	var err error
-	for _, e := range request.InputRoomEvents {
-		msg := &nats.Msg{
-			Subject: r.InputRoomEventTopic,
-			Header:  nats.Header{},
-			Reply:   replyTo,
-		}
-		roomID := e.Event.RoomID()
-		msg.Header.Set("room_id", roomID)
-		if replyTo != "" {
-			msg.Header.Set("sync", replyTo)
-		}
-		msg.Data, err = json.Marshal(e)
-		if err != nil {
-			response.ErrMsg = err.Error()
-			return
-		}
-		if _, err = r.JetStream.PublishMsg(msg); err != nil {
-			logrus.WithError(err).WithFields(logrus.Fields{
-				"room_id":  roomID,
-				"event_id": e.Event.EventID(),
-			}).Error("Roomserver failed to queue async event")
-			return
-		}
-	}
-
-	if request.Asynchronous || replySub == nil {
+	// Queue up the event into the roomserver.
+	replySub, err := r.queueInputRoomEvents(ctx, request)
+	if err != nil {
+		response.ErrMsg = err.Error()
 		return
 	}
 
+	// If we aren't waiting for synchronous responses then we can
+	// give up here, there is nothing further to do.
+	if replySub == nil {
+		return
+	}
+
+	// Otherwise, we'll want to sit and wait for the responses
+	// from the roomserver. There will be one response for every
+	// input we submitted. The last error value we receive will
+	// be the one returned as the error string.
 	defer replySub.Drain() // nolint:errcheck
 	for i := 0; i < len(request.InputRoomEvents); i++ {
 		msg, err := replySub.NextMsgWithContext(ctx)
@@ -207,7 +365,6 @@ func (r *Inputer) InputRoomEvents(
 		}
 		if len(msg.Data) > 0 {
 			response.ErrMsg = string(msg.Data)
-			return
 		}
 	}
 }
diff --git a/roomserver/roomserver.go b/roomserver/roomserver.go
index 896773bab..36e3c5269 100644
--- a/roomserver/roomserver.go
+++ b/roomserver/roomserver.go
@@ -54,8 +54,8 @@ func NewInternalAPI(
 
 	return internal.NewRoomserverAPI(
 		base.ProcessContext, cfg, roomserverDB, js, nc,
-		cfg.Matrix.JetStream.TopicFor(jetstream.InputRoomEvent),
-		cfg.Matrix.JetStream.TopicFor(jetstream.OutputRoomEvent),
+		cfg.Matrix.JetStream.Prefixed(jetstream.InputRoomEvent),
+		cfg.Matrix.JetStream.Prefixed(jetstream.OutputRoomEvent),
 		base.Caches, perspectiveServerNames,
 	)
 }
diff --git a/setup/config/config_jetstream.go b/setup/config/config_jetstream.go
index 9271cd8b4..b6a93d398 100644
--- a/setup/config/config_jetstream.go
+++ b/setup/config/config_jetstream.go
@@ -19,12 +19,12 @@ type JetStream struct {
 	InMemory bool `yaml:"in_memory"`
 }
 
-func (c *JetStream) TopicFor(name string) string {
+func (c *JetStream) Prefixed(name string) string {
 	return fmt.Sprintf("%s%s", c.TopicPrefix, name)
 }
 
 func (c *JetStream) Durable(name string) string {
-	return c.TopicFor(name)
+	return c.Prefixed(name)
 }
 
 func (c *JetStream) Defaults(generate bool) {
diff --git a/setup/jetstream/nats.go b/setup/jetstream/nats.go
index 43cc0331d..748c191b0 100644
--- a/setup/jetstream/nats.go
+++ b/setup/jetstream/nats.go
@@ -1,6 +1,7 @@
 package jetstream
 
 import (
+	"reflect"
 	"strings"
 	"sync"
 	"time"
@@ -75,14 +76,35 @@ func setupNATS(cfg *config.JetStream, nc *natsclient.Conn) (natsclient.JetStream
 	}
 
 	for _, stream := range streams { // streams are defined in streams.go
-		name := cfg.TopicFor(stream.Name)
+		name := cfg.Prefixed(stream.Name)
 		info, err := s.StreamInfo(name)
 		if err != nil && err != natsclient.ErrStreamNotFound {
 			logrus.WithError(err).Fatal("Unable to get stream info")
 		}
+		subjects := stream.Subjects
+		if len(subjects) == 0 {
+			// By default we want each stream to listen for the subjects
+			// that are either an exact match for the stream name, or where
+			// the first part of the subject is the stream name. ">" is a
+			// wildcard in NATS for one or more subject tokens. In the case
+			// that the stream is called "Foo", this will match any message
+			// with the subject "Foo", "Foo.Bar" or "Foo.Bar.Baz" etc.
+			subjects = []string{name, name + ".>"}
+		}
+		if info != nil {
+			switch {
+			case !reflect.DeepEqual(info.Config.Subjects, subjects):
+				fallthrough
+			case info.Config.Retention != stream.Retention:
+				fallthrough
+			case info.Config.Storage != stream.Storage:
+				if err = s.DeleteStream(name); err != nil {
+					logrus.WithError(err).Fatal("Unable to delete stream")
+				}
+				info = nil
+			}
+		}
 		if info == nil {
-			stream.Subjects = []string{name}
-
 			// If we're trying to keep everything in memory (e.g. unit tests)
 			// then overwrite the storage policy.
 			if cfg.InMemory {
@@ -93,8 +115,9 @@ func setupNATS(cfg *config.JetStream, nc *natsclient.Conn) (natsclient.JetStream
 			// array, otherwise we end up with namespaces on namespaces.
 			namespaced := *stream
 			namespaced.Name = name
+			namespaced.Subjects = subjects
 			if _, err = s.AddStream(&namespaced); err != nil {
-				logrus.WithError(err).WithField("stream", name).Fatal("Unable to add stream")
+				logrus.WithError(err).WithField("stream", name).WithField("subjects", subjects).Fatal("Unable to add stream")
 			}
 		}
 	}
diff --git a/setup/jetstream/streams.go b/setup/jetstream/streams.go
index aa3e95cb8..aa979924b 100644
--- a/setup/jetstream/streams.go
+++ b/setup/jetstream/streams.go
@@ -1,6 +1,8 @@
 package jetstream
 
 import (
+	"fmt"
+	"regexp"
 	"time"
 
 	"github.com/nats-io/nats.go"
@@ -24,10 +26,20 @@ var (
 	OutputReadUpdate        = "OutputReadUpdate"
 )
 
+var safeCharacters = regexp.MustCompile("[^A-Za-z0-9$]+")
+
+func Tokenise(str string) string {
+	return safeCharacters.ReplaceAllString(str, "_")
+}
+
+func InputRoomEventSubj(roomID string) string {
+	return fmt.Sprintf("%s.%s", InputRoomEvent, Tokenise(roomID))
+}
+
 var streams = []*nats.StreamConfig{
 	{
 		Name:      InputRoomEvent,
-		Retention: nats.WorkQueuePolicy,
+		Retention: nats.InterestPolicy,
 		Storage:   nats.FileStorage,
 	},
 	{
diff --git a/syncapi/consumers/clientapi.go b/syncapi/consumers/clientapi.go
index fcb7b5b1c..40c1cd3d6 100644
--- a/syncapi/consumers/clientapi.go
+++ b/syncapi/consumers/clientapi.go
@@ -61,7 +61,7 @@ func NewOutputClientDataConsumer(
 	return &OutputClientDataConsumer{
 		ctx:        process.Context(),
 		jetstream:  js,
-		topic:      cfg.Matrix.JetStream.TopicFor(jetstream.OutputClientData),
+		topic:      cfg.Matrix.JetStream.Prefixed(jetstream.OutputClientData),
 		durable:    cfg.Matrix.JetStream.Durable("SyncAPIClientAPIConsumer"),
 		db:         store,
 		notifier:   notifier,
diff --git a/syncapi/consumers/eduserver_receipts.go b/syncapi/consumers/eduserver_receipts.go
index 4e4c61c67..ab79998ea 100644
--- a/syncapi/consumers/eduserver_receipts.go
+++ b/syncapi/consumers/eduserver_receipts.go
@@ -62,7 +62,7 @@ func NewOutputReceiptEventConsumer(
 	return &OutputReceiptEventConsumer{
 		ctx:        process.Context(),
 		jetstream:  js,
-		topic:      cfg.Matrix.JetStream.TopicFor(jetstream.OutputReceiptEvent),
+		topic:      cfg.Matrix.JetStream.Prefixed(jetstream.OutputReceiptEvent),
 		durable:    cfg.Matrix.JetStream.Durable("SyncAPIEDUServerReceiptConsumer"),
 		db:         store,
 		notifier:   notifier,
diff --git a/syncapi/consumers/eduserver_sendtodevice.go b/syncapi/consumers/eduserver_sendtodevice.go
index b0beef063..bdbe77352 100644
--- a/syncapi/consumers/eduserver_sendtodevice.go
+++ b/syncapi/consumers/eduserver_sendtodevice.go
@@ -57,7 +57,7 @@ func NewOutputSendToDeviceEventConsumer(
 	return &OutputSendToDeviceEventConsumer{
 		ctx:        process.Context(),
 		jetstream:  js,
-		topic:      cfg.Matrix.JetStream.TopicFor(jetstream.OutputSendToDeviceEvent),
+		topic:      cfg.Matrix.JetStream.Prefixed(jetstream.OutputSendToDeviceEvent),
 		durable:    cfg.Matrix.JetStream.Durable("SyncAPIEDUServerSendToDeviceConsumer"),
 		db:         store,
 		serverName: cfg.Matrix.ServerName,
diff --git a/syncapi/consumers/eduserver_typing.go b/syncapi/consumers/eduserver_typing.go
index cae5df8a8..c2828c7fc 100644
--- a/syncapi/consumers/eduserver_typing.go
+++ b/syncapi/consumers/eduserver_typing.go
@@ -56,7 +56,7 @@ func NewOutputTypingEventConsumer(
 	return &OutputTypingEventConsumer{
 		ctx:       process.Context(),
 		jetstream: js,
-		topic:     cfg.Matrix.JetStream.TopicFor(jetstream.OutputTypingEvent),
+		topic:     cfg.Matrix.JetStream.Prefixed(jetstream.OutputTypingEvent),
 		durable:   cfg.Matrix.JetStream.Durable("SyncAPIEDUServerTypingConsumer"),
 		eduCache:  eduCache,
 		notifier:  notifier,
diff --git a/syncapi/consumers/roomserver.go b/syncapi/consumers/roomserver.go
index 640c505c2..5bdc0fad7 100644
--- a/syncapi/consumers/roomserver.go
+++ b/syncapi/consumers/roomserver.go
@@ -65,7 +65,7 @@ func NewOutputRoomEventConsumer(
 		ctx:          process.Context(),
 		cfg:          cfg,
 		jetstream:    js,
-		topic:        cfg.Matrix.JetStream.TopicFor(jetstream.OutputRoomEvent),
+		topic:        cfg.Matrix.JetStream.Prefixed(jetstream.OutputRoomEvent),
 		durable:      cfg.Matrix.JetStream.Durable("SyncAPIRoomServerConsumer"),
 		db:           store,
 		notifier:     notifier,
diff --git a/syncapi/consumers/userapi.go b/syncapi/consumers/userapi.go
index a3b2dd53d..010fa7c8e 100644
--- a/syncapi/consumers/userapi.go
+++ b/syncapi/consumers/userapi.go
@@ -56,7 +56,7 @@ func NewOutputNotificationDataConsumer(
 		ctx:       process.Context(),
 		jetstream: js,
 		durable:   cfg.Matrix.JetStream.Durable("SyncAPINotificationDataConsumer"),
-		topic:     cfg.Matrix.JetStream.TopicFor(jetstream.OutputNotificationData),
+		topic:     cfg.Matrix.JetStream.Prefixed(jetstream.OutputNotificationData),
 		db:        store,
 		notifier:  notifier,
 		stream:    stream,
diff --git a/syncapi/syncapi.go b/syncapi/syncapi.go
index f1f827221..ed8118bfc 100644
--- a/syncapi/syncapi.go
+++ b/syncapi/syncapi.go
@@ -67,18 +67,18 @@ func AddPublicRoutes(
 
 	userAPIStreamEventProducer := &producers.UserAPIStreamEventProducer{
 		JetStream: js,
-		Topic:     cfg.Matrix.JetStream.TopicFor(jetstream.OutputStreamEvent),
+		Topic:     cfg.Matrix.JetStream.Prefixed(jetstream.OutputStreamEvent),
 	}
 
 	userAPIReadUpdateProducer := &producers.UserAPIReadProducer{
 		JetStream: js,
-		Topic:     cfg.Matrix.JetStream.TopicFor(jetstream.OutputReadUpdate),
+		Topic:     cfg.Matrix.JetStream.Prefixed(jetstream.OutputReadUpdate),
 	}
 
 	_ = userAPIReadUpdateProducer
 
 	keyChangeConsumer := consumers.NewOutputKeyChangeEventConsumer(
-		process, cfg, cfg.Matrix.JetStream.TopicFor(jetstream.OutputKeyChangeEvent),
+		process, cfg, cfg.Matrix.JetStream.Prefixed(jetstream.OutputKeyChangeEvent),
 		js, keyAPI, rsAPI, syncDB, notifier,
 		streams.DeviceListStreamProvider,
 	)
diff --git a/userapi/consumers/syncapi_readupdate.go b/userapi/consumers/syncapi_readupdate.go
index 2e58020b4..067f93330 100644
--- a/userapi/consumers/syncapi_readupdate.go
+++ b/userapi/consumers/syncapi_readupdate.go
@@ -47,7 +47,7 @@ func NewOutputReadUpdateConsumer(
 		db:           store,
 		ServerName:   cfg.Matrix.ServerName,
 		durable:      cfg.Matrix.JetStream.Durable("UserAPISyncAPIReadUpdateConsumer"),
-		topic:        cfg.Matrix.JetStream.TopicFor(jetstream.OutputReadUpdate),
+		topic:        cfg.Matrix.JetStream.Prefixed(jetstream.OutputReadUpdate),
 		pgClient:     pgClient,
 		userAPI:      userAPI,
 		syncProducer: syncProducer,
diff --git a/userapi/consumers/syncapi_streamevent.go b/userapi/consumers/syncapi_streamevent.go
index 110813274..da3cd3937 100644
--- a/userapi/consumers/syncapi_streamevent.go
+++ b/userapi/consumers/syncapi_streamevent.go
@@ -54,7 +54,7 @@ func NewOutputStreamEventConsumer(
 		jetstream:    js,
 		db:           store,
 		durable:      cfg.Matrix.JetStream.Durable("UserAPISyncAPIStreamEventConsumer"),
-		topic:        cfg.Matrix.JetStream.TopicFor(jetstream.OutputStreamEvent),
+		topic:        cfg.Matrix.JetStream.Prefixed(jetstream.OutputStreamEvent),
 		pgClient:     pgClient,
 		userAPI:      userAPI,
 		rsAPI:        rsAPI,
diff --git a/userapi/userapi.go b/userapi/userapi.go
index 97bdf7b2d..e91ce3a7a 100644
--- a/userapi/userapi.go
+++ b/userapi/userapi.go
@@ -54,8 +54,8 @@ func NewInternalAPI(
 		// it's handled by clientapi, and hence uses its topic. When user
 		// API handles it for all account data, we can remove it from
 		// here.
-		cfg.Matrix.JetStream.TopicFor(jetstream.OutputClientData),
-		cfg.Matrix.JetStream.TopicFor(jetstream.OutputNotificationData),
+		cfg.Matrix.JetStream.Prefixed(jetstream.OutputClientData),
+		cfg.Matrix.JetStream.Prefixed(jetstream.OutputNotificationData),
 	)
 
 	userAPI := &internal.UserInternalAPI{