diff --git a/Cargo.lock b/Cargo.lock
index 45399dec0..083d7ac75 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -689,9 +689,9 @@ dependencies = [
 
 [[package]]
 name = "containers-image-proxy"
-version = "0.9.0"
+version = "0.9.1"
 source = "registry+https://github.com/rust-lang/crates.io-index"
-checksum = "08ca6531917f9b250bf6a1af43603b2e083c192565774451411f9bf4f8bf8f2b"
+checksum = "71a4f5afd361728fbc377e8ec4194040cbd733e9171ff6e35ab31a866ccef1a7"
 dependencies = [
  "cap-std-ext",
  "futures-util",
diff --git a/crates/lib/src/bootc_composefs/status.rs b/crates/lib/src/bootc_composefs/status.rs
index 386e2470a..1c385cdd5 100644
--- a/crates/lib/src/bootc_composefs/status.rs
+++ b/crates/lib/src/bootc_composefs/status.rs
@@ -195,7 +195,7 @@ fn get_sorted_type1_boot_entries_helper(
 pub(crate) async fn get_container_manifest_and_config(
     imgref: &String,
 ) -> Result<ImgConfigManifest> {
-    let config = containers_image_proxy::ImageProxyConfig::default();
+    let config = crate::deploy::new_proxy_config();
     let proxy = containers_image_proxy::ImageProxy::new_with_config(config).await?;
 
     let img = proxy
diff --git a/crates/lib/src/boundimage.rs b/crates/lib/src/boundimage.rs
index a515740bf..31b4e5fb3 100644
--- a/crates/lib/src/boundimage.rs
+++ b/crates/lib/src/boundimage.rs
@@ -121,7 +121,8 @@ pub(crate) fn query_bound_images(root: &Dir) -> Result<Vec<BoundImage>> {
 impl ResolvedBoundImage {
     #[context("resolving bound image {}", src.image)]
     pub(crate) async fn from_image(src: &BoundImage) -> Result<Self> {
-        let proxy = containers_image_proxy::ImageProxy::new().await?;
+        let config = crate::deploy::new_proxy_config();
+        let proxy = containers_image_proxy::ImageProxy::new_with_config(config).await?;
         let img = proxy
             .open_image(&format!("containers-storage:{}", src.image))
             .await?;
diff --git a/crates/lib/src/cli.rs b/crates/lib/src/cli.rs
index 567ba8ddc..d07f190d0 100644
--- a/crates/lib/src/cli.rs
+++ b/crates/lib/src/cli.rs
@@ -26,7 +26,7 @@ use ostree_ext::composefs::fsverity;
 use ostree_ext::composefs::fsverity::FsVerityHashValue;
 use ostree_ext::composefs::splitstream::SplitStreamWriter;
 use ostree_ext::container as ostree_container;
-use ostree_ext::containers_image_proxy::ImageProxyConfig;
+
 use ostree_ext::keyfileext::KeyFileExt;
 use ostree_ext::ostree;
 use ostree_ext::sysroot::SysrootLock;
@@ -1551,7 +1551,7 @@ async fn run_from_opt(opt: Opt) -> Result<()> {
             } => {
                 let (_td_guard, repo) = new_temp_composefs_repo()?;
 
-                let mut proxycfg = ImageProxyConfig::default();
+                let mut proxycfg = crate::deploy::new_proxy_config();
 
                 let image = if let Some(image) = image {
                     image
diff --git a/crates/lib/src/deploy.rs b/crates/lib/src/deploy.rs
index cd90c64f8..766f7acae 100644
--- a/crates/lib/src/deploy.rs
+++ b/crates/lib/src/deploy.rs
@@ -32,6 +32,17 @@ use crate::utils::async_task_with_spinner;
 // TODO use https://github.com/ostreedev/ostree-rs-ext/pull/493/commits/afc1837ff383681b947de30c0cefc70080a4f87a
 const BASE_IMAGE_PREFIX: &str = "ostree/container/baseimage/bootc";
 
+/// Create an ImageProxyConfig with bootc's user agent prefix set.
+///
+/// This allows registries to distinguish "image pulls for bootc client runs"
+/// from other skopeo/containers-image users.
+pub(crate) fn new_proxy_config() -> ostree_ext::containers_image_proxy::ImageProxyConfig {
+    ostree_ext::containers_image_proxy::ImageProxyConfig {
+        user_agent_prefix: Some(format!("bootc/{}", env!("CARGO_PKG_VERSION"))),
+        ..Default::default()
+    }
+}
+
 /// Set on an ostree commit if this is a derived commit
 const BOOTC_DERIVED_KEY: &str = "bootc.derived";
 
@@ -87,7 +98,7 @@ pub(crate) async fn new_importer(
     repo: &ostree::Repo,
     imgref: &ostree_container::OstreeImageReference,
 ) -> Result<ostree_container::store::ImageImporter> {
-    let config = Default::default();
+    let config = new_proxy_config();
     let mut imp = ostree_container::store::ImageImporter::new(repo, imgref, config).await?;
     imp.require_bootable();
     Ok(imp)
@@ -460,7 +471,7 @@ pub(crate) async fn prepare_for_pull_unified(
     let ostree_imgref = OstreeImageReference::from(containers_storage_imgref);
 
     // Configure the importer to use bootc storage as an additional image store
-    let mut config = ostree_ext::containers_image_proxy::ImageProxyConfig::default();
+    let mut config = new_proxy_config();
     let mut cmd = Command::new("skopeo");
     // Use the physical path to bootc storage from the Storage struct
     let storage_path = format!(
@@ -1248,6 +1259,23 @@ pub(crate) fn fixup_etc_fstab(root: &Dir) -> Result<()> {
 mod tests {
     use super::*;
 
+    #[test]
+    fn test_new_proxy_config_user_agent() {
+        let config = new_proxy_config();
+        let prefix = config
+            .user_agent_prefix
+            .expect("user_agent_prefix should be set");
+        assert!(
+            prefix.starts_with("bootc/"),
+            "User agent should start with bootc/"
+        );
+        // Verify the version is present (not just "bootc/")
+        assert!(
+            prefix.len() > "bootc/".len(),
+            "Version should be present after bootc/"
+        );
+    }
+
     #[test]
     fn test_switch_inplace() -> Result<()> {
         use cap_std::fs::DirBuilderExt;
diff --git a/crates/lib/src/install.rs b/crates/lib/src/install.rs
index 00a49581e..0270eda13 100644
--- a/crates/lib/src/install.rs
+++ b/crates/lib/src/install.rs
@@ -932,7 +932,7 @@ async fn install_container(
             }
         };
 
-        let proxy_cfg = ostree_container::store::ImageProxyConfig::default();
+        let proxy_cfg = crate::deploy::new_proxy_config();
         (src_imageref, Some(proxy_cfg))
     };
     let src_imageref = ostree_container::OstreeImageReference {
diff --git a/crates/ostree-ext/Cargo.toml b/crates/ostree-ext/Cargo.toml
index 807131b56..cf1f607d6 100644
--- a/crates/ostree-ext/Cargo.toml
+++ b/crates/ostree-ext/Cargo.toml
@@ -41,7 +41,7 @@ xshell = { workspace = true, optional = true }
 
 # Crate-specific dependencies
 comfy-table = "7.1.1"
-containers-image-proxy = "0.9.0"
+containers-image-proxy = "0.9.1"
 flate2 = { features = ["zlib"], default-features = false, version = "1.0.20" }
 futures-util = "0.3.13"
 gvariant = "0.5.0"
diff --git a/crates/xtask/src/tmt.rs b/crates/xtask/src/tmt.rs
index 0dd4634aa..dbd98dac9 100644
--- a/crates/xtask/src/tmt.rs
+++ b/crates/xtask/src/tmt.rs
@@ -851,7 +851,7 @@ pub(crate) fn update_integration() -> Result<()> {
     // Define tests in order
     let mut tests = vec![];
 
-    // Scan for test-*.nu and test-*.sh files in tmt/tests/booted/
+    // Scan for test-*.nu, test-*.sh, and test-*.py files in tmt/tests/booted/
     let booted_dir = Utf8Path::new("tmt/tests/booted");
 
     for entry in std::fs::read_dir(booted_dir)? {
@@ -862,10 +862,11 @@ pub(crate) fn update_integration() -> Result<()> {
         };
 
         // Extract stem (filename without "test-" prefix and extension)
-        let Some(stem) = filename
-            .strip_prefix("test-")
-            .and_then(|s| s.strip_suffix(".nu").or_else(|| s.strip_suffix(".sh")))
-        else {
+        let Some(stem) = filename.strip_prefix("test-").and_then(|s| {
+            s.strip_suffix(".nu")
+                .or_else(|| s.strip_suffix(".sh"))
+                .or_else(|| s.strip_suffix(".py"))
+        }) else {
             continue;
         };
 
@@ -894,16 +895,16 @@ pub(crate) fn update_integration() -> Result<()> {
             .with_context(|| format!("Failed to get relative path for {}", filename))?;
 
         // Determine test command based on file extension
-        let extension = if filename.ends_with(".nu") {
-            "nu"
+        let test_command = if filename.ends_with(".nu") {
+            format!("nu {}", relative_path.display())
         } else if filename.ends_with(".sh") {
-            "bash"
+            format!("bash {}", relative_path.display())
+        } else if filename.ends_with(".py") {
+            format!("python3 {}", relative_path.display())
         } else {
             anyhow::bail!("Unsupported test file extension: {}", filename);
         };
 
-        let test_command = format!("{} {}", extension, relative_path.display());
-
         // Check if test wants bind storage
         let try_bind_storage = metadata
             .extra
diff --git a/tmt/plans/integration.fmf b/tmt/plans/integration.fmf
index 40ca2135e..3d00102a7 100644
--- a/tmt/plans/integration.fmf
+++ b/tmt/plans/integration.fmf
@@ -71,19 +71,19 @@ execute:
     test:
       - /tmt/tests/tests/test-22-logically-bound-install
 
-/plan-23-usroverlay:
-  summary: Execute tests for bootc usrover
+/plan-23-install-outside-container:
+  summary: Execute tests for installing outside of a container
   discover:
     how: fmf
     test:
-      - /tmt/tests/tests/test-23-usroverlay
+      - /tmt/tests/tests/test-23-install-outside-container
 
-/plan-23-install-outside-container:
-  summary: Execute tests for installing outside of a container
+/plan-23-usroverlay:
+  summary: Execute tests for bootc usrover
   discover:
     how: fmf
     test:
-      - /tmt/tests/tests/test-23-install-outside-container
+      - /tmt/tests/tests/test-23-usroverlay
 
 /plan-24-image-upgrade-reboot:
   summary: Execute local upgrade tests
@@ -166,4 +166,11 @@ execute:
     how: fmf
     test:
       - /tmt/tests/tests/test-33-bib-build
+
+/plan-34-user-agent:
+  summary: Verify bootc sends correct User-Agent header to registries
+  discover:
+    how: fmf
+    test:
+      - /tmt/tests/tests/test-34-user-agent
 # END GENERATED PLANS
diff --git a/tmt/tests/booted/test-user-agent.py b/tmt/tests/booted/test-user-agent.py
new file mode 100644
index 000000000..3eedd9d4b
--- /dev/null
+++ b/tmt/tests/booted/test-user-agent.py
@@ -0,0 +1,230 @@
+#!/usr/bin/env python3
+# number: 34
+# tmt:
+#   summary: Verify bootc sends correct User-Agent header to registries
+#   duration: 10m
+#
+"""
+Test that bootc sends the correct User-Agent header when pulling images.
+
+This test starts a mock HTTP registry server, configures it as an insecure
+registry, and verifies that bootc's requests include "bootc/" in the User-Agent.
+
+Note: The --user-agent-prefix feature requires skopeo >= 1.21.0. If the
+installed skopeo doesn't support it, this test will be skipped.
+
+Note: When insecure=true, container tools first attempt TLS then fall back to
+plain HTTP. Our HTTP server will receive an invalid TLS handshake first, which
+we ignore and continue serving.
+"""
+
+import http.server
+import json
+import os
+import subprocess
+import sys
+import threading
+
+# Global to capture the user agent
+captured_user_agent = None
+server_ready = threading.Event()
+request_received = threading.Event()
+# Global to store the dynamically allocated port
+allocated_port = None
+
+
+def skopeo_supports_user_agent_prefix() -> bool:
+    """Check if the installed skopeo supports --user-agent-prefix."""
+    try:
+        result = subprocess.run(
+            ["skopeo", "--help"],
+            capture_output=True,
+            text=True,
+            timeout=10,
+        )
+        return "--user-agent-prefix" in result.stdout
+    except Exception:
+        return False
+
+
+def parse_os_release() -> dict[str, str]:
+    """Parse /usr/lib/os-release into a dictionary."""
+    os_release = {}
+    try:
+        with open("/usr/lib/os-release") as f:
+            for line in f:
+                line = line.strip()
+                if "=" in line and not line.startswith("#"):
+                    key, _, value = line.partition("=")
+                    # Remove quotes if present
+                    value = value.strip('"\'')
+                    os_release[key] = value
+    except FileNotFoundError:
+        pass
+    return os_release
+
+
+def distro_requires_user_agent_support() -> bool:
+    """Check if the current distro should have skopeo with --user-agent-prefix.
+
+    Returns True if we're on a distro version that ships skopeo >= 1.21.0,
+    meaning the test must not be skipped.
+    """
+    os_release = parse_os_release()
+    distro_id = os_release.get("ID", "")
+    version_id = os_release.get("VERSION_ID", "")
+
+    try:
+        version = int(version_id)
+    except ValueError:
+        return False
+
+    # Fedora 43+ ships skopeo 1.21.0+
+    if distro_id == "fedora" and version >= 43:
+        return True
+
+    return False
+
+
+class RegistryHandler(http.server.BaseHTTPRequestHandler):
+    """Mock registry that captures User-Agent and returns 404."""
+
+    def do_GET(self):
+        global captured_user_agent
+        captured_user_agent = self.headers.get("User-Agent", "")
+        print(f"Request: {self.path}", flush=True)
+        print(f"User-Agent: {captured_user_agent}", flush=True)
+
+        # Return a registry-style 404
+        self.send_response(404)
+        self.send_header("Content-Type", "application/json")
+        body = json.dumps({
+            "errors": [{"code": "NAME_UNKNOWN", "message": "repository not found"}]
+        }).encode()
+        self.send_header("Content-Length", str(len(body)))
+        self.end_headers()
+        self.wfile.write(body)
+        # Signal that we received a valid HTTP request
+        request_received.set()
+
+    def log_message(self, format, *args):
+        print(format % args, flush=True)
+
+
+class TolerantHTTPServer(http.server.HTTPServer):
+    """HTTP server that ignores errors from TLS probe attempts."""
+
+    def handle_error(self, request, client_address):
+        # Silently ignore errors - these are typically TLS handshake attempts
+        # that we can't handle. The client will retry with plain HTTP.
+        print(f"Ignoring error from {client_address} (likely TLS probe)", flush=True)
+
+
+def run_server():
+    """Run the mock registry server on a dynamically allocated port."""
+    global allocated_port
+    # Bind to port 0 to let the OS allocate an available port
+    server = TolerantHTTPServer(("127.0.0.1", 0), RegistryHandler)
+    allocated_port = server.server_address[1]
+    server.timeout = 30
+    server_ready.set()
+    # Handle multiple requests - first few may be TLS probes
+    for _ in range(20):
+        server.handle_request()
+        if captured_user_agent:
+            # Got a valid HTTP request with User-Agent, we're done
+            break
+
+
+def main():
+    # Check if skopeo supports --user-agent-prefix
+    if not skopeo_supports_user_agent_prefix():
+        # Get skopeo version for the skip message
+        try:
+            result = subprocess.run(
+                ["skopeo", "--version"],
+                capture_output=True,
+                text=True,
+                timeout=10,
+            )
+            version = result.stdout.strip()
+        except Exception:
+            version = "unknown"
+
+        # On distros that should have new enough skopeo, fail hard
+        if distro_requires_user_agent_support():
+            print(f"ERROR: skopeo ({version}) does not support --user-agent-prefix", flush=True)
+            print("This distro should have skopeo >= 1.21.0", flush=True)
+            return 1
+
+        print(f"SKIP: skopeo ({version}) does not support --user-agent-prefix", flush=True)
+        print("This feature requires skopeo >= 1.21.0", flush=True)
+        # Exit 0 to skip the test gracefully
+        return 0
+
+    print("=== User-Agent Header Test ===", flush=True)
+
+    # Start server in background thread (port allocated dynamically)
+    server_thread = threading.Thread(target=run_server, daemon=True)
+    server_thread.start()
+
+    # Wait for server to be ready and get the allocated port
+    if not server_ready.wait(timeout=5):
+        print("ERROR: Server failed to start", flush=True)
+        return 1
+
+    registry = f"127.0.0.1:{allocated_port}"
+    print(f"Server listening on {registry}", flush=True)
+
+    # Configure insecure registry
+    registries_conf = f"""[[registry]]
+location = "{registry}"
+insecure = true
+"""
+    conf_path = "/etc/containers/registries.conf.d/99-test-insecure.conf"
+    print(f"Writing registries config to {conf_path}", flush=True)
+    with open(conf_path, "w") as f:
+        f.write(registries_conf)
+    print(registries_conf, flush=True)
+
+    try:
+
+        # Test with bootc
+        print("\n=== Testing with bootc ===", flush=True)
+        result = subprocess.run(
+            ["bootc", "switch", "--transport", "registry", f"{registry}/test:latest"],
+            capture_output=True,
+            text=True,
+            timeout=60,
+        )
+        print(f"bootc exit code: {result.returncode}", flush=True)
+        print(f"bootc stdout: {result.stdout}", flush=True)
+        print(f"bootc stderr: {result.stderr}", flush=True)
+
+        # Wait for server to receive the HTTP request (after TLS probes)
+        if not request_received.wait(timeout=10):
+            print("ERROR: No HTTP request was received by server", flush=True)
+            return 1
+
+        # Check result
+        if not captured_user_agent:
+            print("ERROR: No User-Agent was captured", flush=True)
+            return 1
+
+        print(f"\nCaptured User-Agent: {captured_user_agent}", flush=True)
+
+        if "bootc/" not in captured_user_agent:
+            print(f"ERROR: User-Agent does not contain 'bootc/'", flush=True)
+            return 1
+
+        print("\nSUCCESS: User-Agent contains 'bootc/'", flush=True)
+        return 0
+
+    finally:
+        # Cleanup
+        if os.path.exists(conf_path):
+            os.remove(conf_path)
+
+
+if __name__ == "__main__":
+    sys.exit(main())
diff --git a/tmt/tests/tests.fmf b/tmt/tests/tests.fmf
index 319918962..4d808880e 100644
--- a/tmt/tests/tests.fmf
+++ b/tmt/tests/tests.fmf
@@ -21,16 +21,16 @@
   duration: 30m
   test: nu booted/test-logically-bound-install.nu
 
-/test-23-usroverlay:
-  summary: Execute tests for bootc usrover
-  duration: 30m
-  test: nu booted/test-usroverlay.nu
-
 /test-23-install-outside-container:
   summary: Execute tests for installing outside of a container
   duration: 30m
   test: nu booted/test-install-outside-container.nu
 
+/test-23-usroverlay:
+  summary: Execute tests for bootc usrover
+  duration: 30m
+  test: nu booted/test-usroverlay.nu
+
 /test-24-image-upgrade-reboot:
   summary: Execute local upgrade tests
   duration: 30m
@@ -96,3 +96,8 @@
   require:
   - qemu-img
   test: nu booted/test-bib-build.nu
+
+/test-34-user-agent:
+  summary: Verify bootc sends correct User-Agent header to registries
+  duration: 10m
+  test: python3 booted/test-user-agent.py