diff --git a/src/shared/blockdev-util.c b/src/shared/blockdev-util.c
index bff2047aa1..7ddcb93daf 100644
--- a/src/shared/blockdev-util.c
+++ b/src/shared/blockdev-util.c
@@ -17,9 +17,12 @@
 #include "devnum-util.h"
 #include "dirent-util.h"
 #include "errno-util.h"
+#include "extension-util.h"
 #include "fd-util.h"
 #include "fileio.h"
 #include "fs-util.h"
+#include "macro.h"
+#include "os-util.h"
 #include "parse-util.h"
 #include "path-util.h"
 #include "string-util.h"
@@ -875,6 +878,13 @@ int blockdev_get_root(int level, dev_t *ret) {
                                 return btrfs_log_dev_root(level, r, "/usr");
                         if (r < 0)
                                 return log_full_errno(level, r, "Failed to determine block device of /usr/ file system: %m");
+                        if (r == 0) { /* Not backed by a single block device, we might be looking at a sysext overlay */
+                                r = extension_overlay_block("/usr", IMAGE_SYSEXT, &devno);
+                                if (IN_SET(r, -ENOENT, -ENOTTY))
+                                        r = 0; /* no sysext overlay metadata */
+                                else if (r < 0)
+                                        return log_full_errno(level, r, "Failed to determine backing device of /usr/ extension overlay: %m");
+                        }
                         if (r == 0) { /* /usr/ not backed by single block device, either. */
                                 log_debug("Neither root nor /usr/ file system are on a (single) block device.");
 
diff --git a/src/shared/extension-util.c b/src/shared/extension-util.c
index d993b47de5..e81f2a07ac 100644
--- a/src/shared/extension-util.c
+++ b/src/shared/extension-util.c
@@ -12,6 +12,7 @@
 #include "fd-util.h"
 #include "fileio.h"
 #include "log.h"
+#include "macro.h"
 #include "os-util.h"
 #include "path-util.h"
 #include "stat-util.h"
@@ -192,6 +193,7 @@ int extension_overlay_block(const char *p, ImageClass image_class, dev_t *ret) {
 
         assert(p);
         assert(ret);
+        assert(IN_SET(image_class, IMAGE_SYSEXT, IMAGE_CONFEXT));
 
         /* Tries to read the backing device information systemd-sysext puts in
          * the virtual file .systemd-sysext/.systemd-confext */
diff --git a/test/units/TEST-50-DISSECT.usr-gpt-auto-generator.sh b/test/units/TEST-50-DISSECT.usr-gpt-auto-generator.sh
new file mode 100755
index 0000000000..37a85e1865
--- /dev/null
+++ b/test/units/TEST-50-DISSECT.usr-gpt-auto-generator.sh
@@ -0,0 +1,93 @@
+#!/usr/bin/env bash
+# SPDX-License-Identifier: LGPL-2.1-or-later
+set -eux
+set -o pipefail
+
+GENERATOR_BIN="/usr/lib/systemd/system-generators/systemd-gpt-auto-generator"
+WORK_DIR="$(mktemp --directory /var/tmp/test-gpt-auto-generator.XXXXXX)"
+DEFINITIONS="$WORK_DIR/definitions"
+IMAGE="$WORK_DIR/image.raw"
+OUTPUT="$WORK_DIR/output"
+ROOT="$WORK_DIR/root"
+LOOP=""
+
+at_exit() {
+    set +e
+
+    if [[ -n "$LOOP" ]]; then
+        losetup --detach "$LOOP"
+    fi
+
+    rm -rf "$WORK_DIR"
+}
+
+trap at_exit EXIT
+
+test -x "$GENERATOR_BIN"
+mkdir -p "$DEFINITIONS" "$OUTPUT"/{normal,early,late} "$ROOT"
+
+cat >"$DEFINITIONS/10-usr.conf" <<EOF
+[Partition]
+Type=usr
+SizeMinBytes=10M
+SizeMaxBytes=10M
+EOF
+
+cat >"$DEFINITIONS/20-home.conf" <<EOF
+[Partition]
+Type=home
+SizeMinBytes=10M
+SizeMaxBytes=10M
+EOF
+
+systemd-repart \
+    --definitions="$DEFINITIONS" \
+    --empty=create \
+    --size=32M \
+    --dry-run=no \
+    --offline=yes \
+    "$IMAGE"
+
+LOOP="$(losetup --show --find --partscan "$IMAGE")"
+udevadm wait --timeout=60 --settle --initialized=no "$LOOP"p1 "$LOOP"p2
+
+# Recreate a root=tmpfs system whose /usr/ is backed by a GPT partition and overlaid by systemd-sysext.
+# Run the generator as PID 1 because generators deliberately do nothing in containers.
+unshare --mount --pid --fork --mount-proc \
+    bash -euxo pipefail -s -- "$ROOT" "$OUTPUT" "$WORK_DIR" "$LOOP" "$GENERATOR_BIN" <<'EOF'
+mount --make-rprivate /
+
+mount --types tmpfs tmpfs "$1"
+mkdir -p "$1"/{dev,proc,run/generator-output,sys,usr}
+mount --bind /dev "$1/dev"
+mount --bind /proc "$1/proc"
+mount --bind /sys "$1/sys"
+mount --bind "$2" "$1/run/generator-output"
+
+mkdir -p "$3/usr-upper" "$3/usr-work"
+mount --types overlay overlay \
+    --options lowerdir=/usr,upperdir="$3/usr-upper",workdir="$3/usr-work" \
+    "$1/usr"
+
+for directory in bin lib lib64 sbin; do
+    if [[ -e "/$directory" ]]; then
+        mkdir -p "$1/$directory"
+        mount --bind "/$directory" "$1/$directory"
+    fi
+done
+
+mkdir -p "$1/usr/.systemd-sysext"
+cat "/sys/class/block/${4##*/}p1/dev" >"$1/usr/.systemd-sysext/backing"
+
+export container=
+export SYSTEMD_IN_INITRD=0
+export SYSTEMD_PROC_CMDLINE="root=tmpfs systemd.gpt_auto=yes"
+exec chroot "$1" "$5" \
+    /run/generator-output/normal \
+    /run/generator-output/early \
+    /run/generator-output/late
+EOF
+
+test -f "$OUTPUT/late/home.mount"
+WHAT="$(sed -n 's/^What=//p' "$OUTPUT/late/home.mount")"
+test "$(readlink --canonicalize "$WHAT")" = "$(readlink --canonicalize "${LOOP}p2")"