diff --git a/hw/9pfs/9p-local.c b/hw/9pfs/9p-local.c
index 1a5e3eed73..7137a28109 100644
--- a/hw/9pfs/9p-local.c
+++ b/hw/9pfs/9p-local.c
@@ -559,6 +559,15 @@ static struct dirent *local_readdir(FsContext *ctx, V9fsFidOpenState *fs)
 
 again:
     entry = readdir(fs->dir.stream);
+#ifdef CONFIG_DARWIN
+    int td;
+    td = telldir(fs->dir.stream);
+    /* If telldir fails, fail the entire readdir call */
+    if (td < 0) {
+        return NULL;
+    }
+    entry->d_seekoff = td;
+#endif
     if (!entry) {
         return NULL;
     }
diff --git a/hw/9pfs/9p-proxy.c b/hw/9pfs/9p-proxy.c
index b1664080d8..8b4b5cf7dc 100644
--- a/hw/9pfs/9p-proxy.c
+++ b/hw/9pfs/9p-proxy.c
@@ -706,7 +706,21 @@ static off_t proxy_telldir(FsContext *ctx, V9fsFidOpenState *fs)
 
 static struct dirent *proxy_readdir(FsContext *ctx, V9fsFidOpenState *fs)
 {
-    return readdir(fs->dir.stream);
+    struct dirent *entry;
+    entry = readdir(fs->dir.stream);
+#ifdef CONFIG_DARWIN
+    if (!entry) {
+        return NULL;
+    }
+    int td;
+    td = telldir(fs->dir.stream);
+    /* If telldir fails, fail the entire readdir call */
+    if (td < 0) {
+        return NULL;
+    }
+    entry->d_seekoff = td;
+#endif
+    return entry;
 }
 
 static void proxy_seekdir(FsContext *ctx, V9fsFidOpenState *fs, off_t off)
diff --git a/hw/9pfs/9p-synth.c b/hw/9pfs/9p-synth.c
index 4a4a776d06..e264a03eef 100644
--- a/hw/9pfs/9p-synth.c
+++ b/hw/9pfs/9p-synth.c
@@ -222,7 +222,11 @@ static void synth_direntry(V9fsSynthNode *node,
 {
     strcpy(entry->d_name, node->name);
     entry->d_ino = node->attr->inode;
+#ifdef CONFIG_DARWIN
+    entry->d_seekoff = off + 1;
+#else
     entry->d_off = off + 1;
+#endif
 }
 
 static struct dirent *synth_get_dentry(V9fsSynthNode *dir,
diff --git a/hw/9pfs/9p-util.h b/hw/9pfs/9p-util.h
index 546f46dc7d..accbec9987 100644
--- a/hw/9pfs/9p-util.h
+++ b/hw/9pfs/9p-util.h
@@ -79,3 +79,20 @@ ssize_t fremovexattrat_nofollow(int dirfd, const char *filename,
                                 const char *name);
 
 #endif
+
+
+/**
+ * Darwin has d_seekoff, which appears to function similarly to d_off.
+ * However, it does not appear to be supported on all file systems,
+ * so ensure it is manually injected earlier and call here when
+ * needed.
+ */
+
+inline off_t qemu_dirent_off(struct dirent *dent)
+{
+#ifdef CONFIG_DARWIN
+    return dent->d_seekoff;
+#else
+    return dent->d_off;
+#endif
+}
diff --git a/hw/9pfs/9p.c b/hw/9pfs/9p.c
index 1563d7b7c6..cf694da354 100644
--- a/hw/9pfs/9p.c
+++ b/hw/9pfs/9p.c
@@ -27,6 +27,7 @@
 #include "virtio-9p.h"
 #include "fsdev/qemu-fsdev.h"
 #include "9p-xattr.h"
+#include "9p-util.h"
 #include "coth.h"
 #include "trace.h"
 #include "migration/blocker.h"
@@ -2281,7 +2282,11 @@ static int coroutine_fn v9fs_do_readdir_with_stat(V9fsPDU *pdu,
         count += len;
         v9fs_stat_free(&v9stat);
         v9fs_path_free(&path);
-        saved_dir_pos = dent->d_off;
+        saved_dir_pos = qemu_dirent_off(dent);
+        if (saved_dir_pos < 0) {
+            err = saved_dir_pos;
+            break;
+        }
     }
 
     v9fs_readdir_unlock(&fidp->fs.dir);
@@ -2420,6 +2425,7 @@ static int coroutine_fn v9fs_do_readdir(V9fsPDU *pdu, V9fsFidState *fidp,
     V9fsString name;
     int len, err = 0;
     int32_t count = 0;
+    off_t off;
     struct dirent *dent;
     struct stat *st;
     struct V9fsDirEnt *entries = NULL;
@@ -2480,12 +2486,17 @@ static int coroutine_fn v9fs_do_readdir(V9fsPDU *pdu, V9fsFidState *fidp,
             qid.version = 0;
         }
 
+        off = qemu_dirent_off(dent);
+        if (off < 0) {
+            err = off;
+            break;
+        }
         v9fs_string_init(&name);
         v9fs_string_sprintf(&name, "%s", dent->d_name);
 
         /* 11 = 7 + 4 (7 = start offset, 4 = space for storing count) */
         len = pdu_marshal(pdu, 11 + count, "Qqbs",
-                          &qid, dent->d_off,
+                          &qid, off,
                           dent->d_type, &name);
 
         v9fs_string_free(&name);
diff --git a/hw/9pfs/codir.c b/hw/9pfs/codir.c
index 032cce04c4..fac6759a64 100644
--- a/hw/9pfs/codir.c
+++ b/hw/9pfs/codir.c
@@ -167,7 +167,14 @@ static int do_readdir_many(V9fsPDU *pdu, V9fsFidState *fidp,
         }
 
         size += len;
+        /* This conditional statement is identical in
+         * function to qemu_dirent_off, described in 9p-util.h,
+         * since that header cannot be included here. */
+#ifdef CONFIG_DARWIN
+        saved_dir_pos = dent->d_seekoff;
+#else
         saved_dir_pos = dent->d_off;
+#endif
     }
 
     /* restore (last) saved position */
