diff --git a/server/filestore.go b/server/filestore.go
index 82d3124a..77a6a2f5 100644
--- a/server/filestore.go
+++ b/server/filestore.go
@@ -2153,7 +2153,8 @@ func (fs *fileStore) removeMsg(seq uint64, secure, needFSLock bool) (bool, error
 	if firstSeqNeedsUpdate {
 		fs.selectNextFirst()
 		// Write out the new first message block if we have one.
-		if len(fs.blks) > 0 {
+		// We can ignore if we really have not changed message blocks from above.
+		if len(fs.blks) > 0 && fs.blks[0] != mb {
 			fmb := fs.blks[0]
 			fmb.writeIndexInfo()
 		}
@@ -4030,6 +4031,14 @@ func (mb *msgBlock) writeIndexInfoLocked() error {
 
 	mb.lwits = time.Now().UnixNano()
 
+	// Check if this will be a short write, and if so truncate before writing here.
+	if int64(len(buf)) < mb.liwsz {
+		if err := mb.ifd.Truncate(0); err != nil {
+			mb.werr = err
+			return err
+		}
+	}
+
 	var err error
 	if n, err = mb.ifd.WriteAt(buf, 0); err == nil {
 		mb.liwsz = int64(n)
@@ -4682,10 +4691,10 @@ func (mb *msgBlock) closeAndKeepIndex() {
 		// We were closed, so just write out an empty file.
 		ioutil.WriteFile(mb.mfn, nil, defaultFilePerms)
 	}
-	// Close
-	mb.dirtyCloseWithRemove(false)
 	// Make sure to write the index file so we can remember last seq and ts.
 	mb.writeIndexInfoLocked()
+	// Close
+	mb.dirtyCloseWithRemove(false)
 
 	// Clear any fss.
 	if mb.sfn != _EMPTY_ {
diff --git a/server/filestore_test.go b/server/filestore_test.go
index 9249199c..6b905312 100644
--- a/server/filestore_test.go
+++ b/server/filestore_test.go
@@ -3907,3 +3907,71 @@ func TestFileStorePurgeExWithSubject(t *testing.T) {
 	fs.PurgeEx("foo", 1, 0)
 	require_True(t, fs.State().Msgs == 0)
 }
+
+// When the N.idx file is shorter than the previous write we could fail to recover the idx properly.
+// For instance, with encryption and an expiring stream that has no messages, when a restart happens the decrypt will fail
+// since their are extra bytes, and this could lead to a stream sequence reset to zero.
+func TestFileStoreShortIndexWriteBug(t *testing.T) {
+	storeDir := createDir(t, JetStreamStoreDir)
+	defer removeDir(t, storeDir)
+
+	// Encrypted mode shows, but could effect non-encrypted mode.
+	prf := func(context []byte) ([]byte, error) {
+		h := hmac.New(sha256.New, []byte("offby1"))
+		if _, err := h.Write(context); err != nil {
+			return nil, err
+		}
+		return h.Sum(nil), nil
+	}
+
+	created := time.Now()
+
+	fs, err := newFileStoreWithCreated(
+		FileStoreConfig{StoreDir: storeDir},
+		StreamConfig{Name: "TEST", Storage: FileStorage, MaxAge: time.Second},
+		created,
+		prf,
+	)
+	require_NoError(t, err)
+	defer fs.Stop()
+
+	for i := 0; i < 100; i++ {
+		_, _, err = fs.StoreMsg("foo", nil, nil)
+		require_NoError(t, err)
+	}
+	// Wait til messages all go away.
+	checkFor(t, 2*time.Second, 200*time.Millisecond, func() error {
+		if state := fs.State(); state.Msgs != 0 {
+			return fmt.Errorf("Expected no msgs, got %d", state.Msgs)
+		}
+		return nil
+	})
+
+	if state := fs.State(); state.FirstSeq != 101 {
+		t.Fatalf("Expected first sequence of 101 vs %d", state.FirstSeq)
+	}
+
+	// I noticed that we also would dangle an open ifd when we did closeAndKeepIndex(), check that we do not anymore.
+	fs.mu.RLock()
+	mb := fs.lmb
+	mb.mu.RLock()
+	hasIfd := mb.ifd != nil
+	mb.mu.RUnlock()
+	fs.mu.RUnlock()
+	require_False(t, hasIfd)
+
+	// Now restart..
+	fs.Stop()
+	fs, err = newFileStoreWithCreated(
+		FileStoreConfig{StoreDir: storeDir},
+		StreamConfig{Name: "TEST", Storage: FileStorage, MaxAge: time.Second},
+		created,
+		prf,
+	)
+	require_NoError(t, err)
+	defer fs.Stop()
+
+	if state := fs.State(); state.FirstSeq != 101 {
+		t.Fatalf("Expected first sequence of 101 vs %d", state.FirstSeq)
+	}
+}