diff --git a/migration/file.c b/migration/file.c
index a903710f06..db870f2cf0 100644
--- a/migration/file.c
+++ b/migration/file.c
@@ -50,12 +50,31 @@ void file_cleanup_outgoing_migration(void)
     outgoing_args.fname = NULL;
 }
 
+static void file_enable_direct_io(int *flags)
+{
+#ifdef O_DIRECT
+    *flags |= O_DIRECT;
+#else
+    /* it should have been rejected when setting the parameter */
+    g_assert_not_reached();
+#endif
+}
+
 bool file_send_channel_create(gpointer opaque, Error **errp)
 {
     QIOChannelFile *ioc;
     int flags = O_WRONLY;
     bool ret = true;
 
+    if (migrate_direct_io()) {
+        /*
+         * Enable O_DIRECT for the secondary channels. These are used
+         * for sending ram pages and writes should be guaranteed to be
+         * aligned to at least page size.
+         */
+        file_enable_direct_io(&flags);
+    }
+
     ioc = qio_channel_file_new_path(outgoing_args.fname, flags, 0, errp);
     if (!ioc) {
         ret = false;
@@ -117,21 +136,25 @@ static gboolean file_accept_incoming_migration(QIOChannel *ioc,
     return G_SOURCE_REMOVE;
 }
 
-void file_create_incoming_channels(QIOChannel *ioc, Error **errp)
+static void file_create_incoming_channels(QIOChannel *ioc, char *filename,
+                                          Error **errp)
 {
-    int i, fd, channels = 1;
+    int i, channels = 1;
     g_autofree QIOChannel **iocs = NULL;
+    int flags = O_RDONLY;
 
     if (migrate_multifd()) {
         channels += migrate_multifd_channels();
+        if (migrate_direct_io()) {
+            file_enable_direct_io(&flags);
+        }
     }
 
     iocs = g_new0(QIOChannel *, channels);
-    fd = QIO_CHANNEL_FILE(ioc)->fd;
     iocs[0] = ioc;
 
     for (i = 1; i < channels; i++) {
-        QIOChannelFile *fioc = qio_channel_file_new_dupfd(fd, errp);
+        QIOChannelFile *fioc = qio_channel_file_new_path(filename, flags, 0, errp);
 
         if (!fioc) {
             while (i) {
@@ -171,7 +194,7 @@ void file_start_incoming_migration(FileMigrationArgs *file_args, Error **errp)
         return;
     }
 
-    file_create_incoming_channels(QIO_CHANNEL(fioc), errp);
+    file_create_incoming_channels(QIO_CHANNEL(fioc), filename, errp);
 }
 
 int file_write_ramblock_iov(QIOChannel *ioc, const struct iovec *iov,
diff --git a/migration/file.h b/migration/file.h
index 7699c04677..9f71e87f74 100644
--- a/migration/file.h
+++ b/migration/file.h
@@ -20,7 +20,6 @@ void file_start_outgoing_migration(MigrationState *s,
 int file_parse_offset(char *filespec, uint64_t *offsetp, Error **errp);
 void file_cleanup_outgoing_migration(void);
 bool file_send_channel_create(gpointer opaque, Error **errp);
-void file_create_incoming_channels(QIOChannel *ioc, Error **errp);
 int file_write_ramblock_iov(QIOChannel *ioc, const struct iovec *iov,
                             int niov, RAMBlock *block, Error **errp);
 int multifd_file_recv_data(MultiFDRecvParams *p, Error **errp);
diff --git a/migration/migration.c b/migration/migration.c
index e1b269624c..e03c80b3aa 100644
--- a/migration/migration.c
+++ b/migration/migration.c
@@ -155,6 +155,16 @@ static bool migration_needs_seekable_channel(void)
     return migrate_mapped_ram();
 }
 
+static bool migration_needs_extra_fds(void)
+{
+    /*
+     * When doing direct-io, multifd requires two different,
+     * non-duplicated file descriptors so we can use one of them for
+     * unaligned IO.
+     */
+    return migrate_multifd() && migrate_direct_io();
+}
+
 static bool transport_supports_seeking(MigrationAddress *addr)
 {
     if (addr->transport == MIGRATION_ADDRESS_TYPE_FILE) {
@@ -164,6 +174,12 @@ static bool transport_supports_seeking(MigrationAddress *addr)
     return false;
 }
 
+static bool transport_supports_extra_fds(MigrationAddress *addr)
+{
+    /* file: works because QEMU can open it multiple times */
+    return addr->transport == MIGRATION_ADDRESS_TYPE_FILE;
+}
+
 static bool
 migration_channels_and_transport_compatible(MigrationAddress *addr,
                                             Error **errp)
@@ -180,6 +196,13 @@ migration_channels_and_transport_compatible(MigrationAddress *addr,
         return false;
     }
 
+    if (migration_needs_extra_fds() &&
+        !transport_supports_extra_fds(addr)) {
+        error_setg(errp,
+                   "Migration requires a transport that allows for extra fds (e.g. file)");
+        return false;
+    }
+
     return true;
 }