diff --git a/refs.c b/refs.c
index 58b118243c..85c1dcb017 100644
--- a/refs.c
+++ b/refs.c
@@ -30,6 +30,13 @@ static unsigned char refname_disposition[256] = {
  * pruned.
  */
 #define REF_ISPRUNING	0x0100
+
+/*
+ * Used as a flag in ref_update::flags when the lockfile needs to be
+ * committed.
+ */
+#define REF_NEEDS_COMMIT 0x0200
+
 /*
  * Try to read one refname component from the front of refname.
  * Return the length of the component found, or -1 if the component is
@@ -3799,7 +3806,12 @@ int ref_transaction_commit(struct ref_transaction *transaction,
 		goto cleanup;
 	}
 
-	/* Acquire all locks while verifying old values */
+	/*
+	 * Acquire all locks, verify old values if provided, check
+	 * that new values are valid, and write new values to the
+	 * lockfiles, ready to be activated. Only keep one lockfile
+	 * open at a time to avoid running out of file descriptors.
+	 */
 	for (i = 0; i < n; i++) {
 		struct ref_update *update = updates[i];
 
@@ -3820,26 +3832,49 @@ int ref_transaction_commit(struct ref_transaction *transaction,
 				    update->refname);
 			goto cleanup;
 		}
+		if (!(update->flags & REF_DELETING) &&
+		    (update->lock->force_write ||
+		     hashcmp(update->lock->old_sha1, update->new_sha1))) {
+			if (write_ref_to_lockfile(update->lock, update->new_sha1)) {
+				/*
+				 * The lock was freed upon failure of
+				 * write_ref_to_lockfile():
+				 */
+				update->lock = NULL;
+				strbuf_addf(err, "Cannot update the ref '%s'.",
+					    update->refname);
+				ret = TRANSACTION_GENERIC_ERROR;
+				goto cleanup;
+			}
+			update->flags |= REF_NEEDS_COMMIT;
+		} else {
+			/*
+			 * We didn't have to write anything to the lockfile.
+			 * Close it to free up the file descriptor:
+			 */
+			if (close_ref(update->lock)) {
+				strbuf_addf(err, "Couldn't close %s.lock",
+					    update->refname);
+				goto cleanup;
+			}
+		}
 	}
 
 	/* Perform updates first so live commits remain referenced */
 	for (i = 0; i < n; i++) {
 		struct ref_update *update = updates[i];
 
-		if (!(update->flags & REF_DELETING)) {
-			if (!update->lock->force_write &&
-			    !hashcmp(update->lock->old_sha1, update->new_sha1)) {
-				unlock_ref(update->lock);
+		if (update->flags & REF_NEEDS_COMMIT) {
+			if (commit_ref_update(update->lock,
+					      update->new_sha1, update->msg)) {
+				/* The lock was freed by commit_ref_update(): */
 				update->lock = NULL;
-			} else if (write_ref_to_lockfile(update->lock, update->new_sha1) ||
-				   commit_ref_update(update->lock, update->new_sha1, update->msg)) {
-				update->lock = NULL; /* freed by the above calls */
 				strbuf_addf(err, "Cannot update the ref '%s'.",
 					    update->refname);
 				ret = TRANSACTION_GENERIC_ERROR;
 				goto cleanup;
 			} else {
-				/* freed by the above calls: */
+				/* freed by the above call: */
 				update->lock = NULL;
 			}
 		}
@@ -3849,7 +3884,7 @@ int ref_transaction_commit(struct ref_transaction *transaction,
 	for (i = 0; i < n; i++) {
 		struct ref_update *update = updates[i];
 
-		if (update->lock) {
+		if (update->flags & REF_DELETING) {
 			if (delete_ref_loose(update->lock, update->type, err)) {
 				ret = TRANSACTION_GENERIC_ERROR;
 				goto cleanup;
diff --git a/t/t1400-update-ref.sh b/t/t1400-update-ref.sh
index 47d2fe9cce..c593a1df20 100755
--- a/t/t1400-update-ref.sh
+++ b/t/t1400-update-ref.sh
@@ -979,7 +979,7 @@ run_with_limited_open_files () {
 
 test_lazy_prereq ULIMIT_FILE_DESCRIPTORS 'run_with_limited_open_files true'
 
-test_expect_failure ULIMIT_FILE_DESCRIPTORS 'large transaction creating branches does not burst open file limit' '
+test_expect_success ULIMIT_FILE_DESCRIPTORS 'large transaction creating branches does not burst open file limit' '
 (
 	for i in $(test_seq 33)
 	do
@@ -990,7 +990,7 @@ test_expect_failure ULIMIT_FILE_DESCRIPTORS 'large transaction creating branches
 )
 '
 
-test_expect_failure ULIMIT_FILE_DESCRIPTORS 'large transaction deleting branches does not burst open file limit' '
+test_expect_success ULIMIT_FILE_DESCRIPTORS 'large transaction deleting branches does not burst open file limit' '
 (
 	for i in $(test_seq 33)
 	do