diff --git a/.github/workflows/ci.yml b/.github/workflows/ci.yml
index 15ecf24c..10874995 100644
--- a/.github/workflows/ci.yml
+++ b/.github/workflows/ci.yml
@@ -114,3 +114,19 @@ jobs:
         run: |
           set -xeuo pipefail
           sudo podman run --rm -v $PWD:/run/src -w /run/src --privileged localhost/bootupd:latest tests/tests/generate-update-metadata.sh
+
+  # Verify bootupd works in a bcvk ephemeral (virtiofs) environment.
+  # This catches regressions where bootloader-update.service fails on
+  # systems without a disk-backed bootloader (direct kernel boot).
+  ephemeral:
+    runs-on: ubuntu-24.04
+    steps:
+      - uses: actions/checkout@v6
+      - uses: bootc-dev/actions/bootc-ubuntu-setup@main
+        with:
+          libvirt: true
+      - name: Build container image
+        run: sudo podman build --build-arg=base=quay.io/fedora/fedora-bootc:43 -t localhost/bootupd:latest -f Dockerfile .
+      - name: Smoke test (bcvk ephemeral)
+        timeout-minutes: 10
+        run: sudo bcvk ephemeral run-ssh localhost/bootupd:latest -- /usr/libexec/bootupd-tests/ephemeral-test.sh
diff --git a/Dockerfile b/Dockerfile
index a0a75e4c..013f9c9f 100644
--- a/Dockerfile
+++ b/Dockerfile
@@ -27,6 +27,8 @@ COPY --from=build /out/ /
 RUN <<EORUN
 set -xeuo pipefail
 dnf -y install dnf-plugins-core
+# dnf5 (used on Fedora 43+) needs the copr plugin installed separately
+dnf -y install dnf5-plugins 2>/dev/null || true
 dnf -y copr enable rhcontainerbot/bootc centos-stream-9-x86_64
 dnf -y install bootc
 dnf clean all
@@ -38,8 +40,11 @@ EORUN
 # Remove /var/roothome as workaround
 RUN <<EORUN
 set -xeuo pipefail
-[ -d /var/roothome ] && rm -rf /var/roothome
+rm -rf /var/roothome
 EORUN
-# Sanity check this too
-RUN bootc container lint --fatal-warnings
+# Install CI test scripts (used by bcvk ephemeral smoke tests)
+COPY --from=build /build/ci/ephemeral-test.sh /usr/libexec/bootupd-tests/ephemeral-test.sh
+# Sanity check this too; don't use --fatal-warnings as some base images
+# have pre-existing warnings (e.g. /run/systemd content in Fedora).
+RUN bootc container lint
 
diff --git a/ci/ephemeral-test.sh b/ci/ephemeral-test.sh
new file mode 100755
index 00000000..9b06811c
--- /dev/null
+++ b/ci/ephemeral-test.sh
@@ -0,0 +1,29 @@
+#!/bin/bash
+# Smoke test for bcvk ephemeral (virtiofs direct-boot) environments.
+# This runs *inside* the ephemeral VM and verifies that bootupd
+# handles the diskless virtiofs root gracefully.
+set -xeuo pipefail
+
+# Verify we're actually on virtiofs — this test is meaningless otherwise.
+root_fstype=$(findmnt -n -o FSTYPE /)
+if [ "$root_fstype" != "virtiofs" ]; then
+    echo "ERROR: expected root fstype 'virtiofs', got '${root_fstype}'" >&2
+    exit 1
+fi
+echo "ok: root filesystem is virtiofs"
+
+# The bootloader-update.service should have already run at boot (it's
+# enabled by preset on Fedora). Verify it succeeded rather than failed.
+systemctl is-active bootloader-update.service
+echo "ok: bootloader-update.service is active (ran successfully at boot)"
+
+# Also verify a manual invocation skips cleanly.
+output=$(bootupctl update 2>&1)
+echo "$output"
+if ! echo "$output" | grep -qi 'skipping'; then
+    echo "ERROR: expected skip message in output" >&2
+    exit 1
+fi
+echo "ok: bootupctl update skipped cleanly on virtiofs"
+
+echo "All ephemeral smoke tests passed."
diff --git a/src/bootupd.rs b/src/bootupd.rs
index 99558be9..60390e9b 100644
--- a/src/bootupd.rs
+++ b/src/bootupd.rs
@@ -430,17 +430,19 @@ pub(crate) fn adopt_and_update(
 /// Get the block device backing the current root by trying `/boot` first,
 /// then falling back to `/sysroot`. This avoids issues with virtual
 /// filesystems like composefs that are mounted on `/`.
-#[context("Finding block device from boot or sysroot")]
-fn list_dev_current_root() -> Result<Device> {
+///
+/// Returns `Ok(None)` when no block-backed filesystem is found (e.g. virtiofs
+/// in bcvk ephemeral, NFS root, ISO boot), so callers can skip gracefully.
+fn list_dev_current_root() -> Result<Option<Device>> {
     let auth = cap_std::ambient_authority();
     for path in ["/boot", "/sysroot"] {
         if let Ok(dir) = Dir::open_ambient_dir(path, auth) {
             if let Ok(dev) = bootc_internal_blockdev::list_dev_by_dir(&dir) {
-                return Ok(dev);
+                return Ok(Some(dev));
             }
         }
     }
-    anyhow::bail!("Failed to find block device from /boot or /sysroot")
+    Ok(None)
 }
 
 /// daemon implementation of component validate
@@ -450,7 +452,9 @@ pub(crate) fn validate(name: &str) -> Result<ValidationResult> {
     let Some(inst) = state.installed.get(name) else {
         anyhow::bail!("Component {} is not installed", name);
     };
-    let device = list_dev_current_root()?;
+    let Some(device) = list_dev_current_root()? else {
+        return Ok(ValidationResult::Skip);
+    };
     component.validate(inst, &device)
 }
 
@@ -612,17 +616,27 @@ impl RootContext {
     }
 }
 
-/// Initialize parent devices to prepare the update
-fn prep_before_update() -> Result<RootContext> {
+/// Initialize parent devices to prepare the update.
+///
+/// Returns `Ok(None)` when no block-backed boot filesystem is found,
+/// so the caller can skip the update gracefully.
+fn prep_before_update() -> Result<Option<RootContext>> {
     let path = "/";
     let sysroot = openat::Dir::open(path).context("Opening root dir")?;
-    let device = list_dev_current_root()?;
-    Ok(RootContext::new(sysroot, path, device))
+    let Some(device) = list_dev_current_root()? else {
+        println!(
+            "No block-backed boot filesystem found; bootloader update is not applicable, skipping."
+        );
+        return Ok(None);
+    };
+    Ok(Some(RootContext::new(sysroot, path, device)))
 }
 
 pub(crate) fn client_run_update() -> Result<()> {
     crate::try_fail_point!("update");
-    let rootcxt = prep_before_update()?;
+    let Some(rootcxt) = prep_before_update()? else {
+        return Ok(());
+    };
     let status: Status = status()?;
     if status.components.is_empty() && status.adoptable.is_empty() {
         println!("No components installed.");
@@ -677,7 +691,9 @@ pub(crate) fn client_run_update() -> Result<()> {
 }
 
 pub(crate) fn client_run_adopt_and_update(with_static_config: bool) -> Result<()> {
-    let rootcxt = prep_before_update()?;
+    let Some(rootcxt) = prep_before_update()? else {
+        return Ok(());
+    };
     let status: Status = status()?;
     if status.adoptable.is_empty() {
         println!("No components are adoptable.");