diff --git a/e2e/configs/gateway/docker.toml b/e2e/configs/gateway/docker.toml
new file mode 100644
index 0000000000..008ed65316
--- /dev/null
+++ b/e2e/configs/gateway/docker.toml
@@ -0,0 +1,27 @@
+# SPDX-FileCopyrightText: Copyright (c) 2025-2026 NVIDIA CORPORATION & AFFILIATES. All rights reserved.
+# SPDX-License-Identifier: Apache-2.0
+
+[openshell]
+version = 1
+
+[openshell.gateway]
+bind_address = "127.0.0.1:8080"
+log_level = "info"
+compute_drivers = ["docker"]
+disable_tls = true
+
+[openshell.gateway.auth]
+allow_unauthenticated_users = true
+
+[openshell.gateway.gateway_jwt]
+signing_key_path = ".cache/openshell-e2e/gateway-jwt/signing.pem"
+public_key_path = ".cache/openshell-e2e/gateway-jwt/public.pem"
+kid_path = ".cache/openshell-e2e/gateway-jwt/kid"
+gateway_id = "openshell-e2e"
+ttl_secs = 0
+
+[openshell.drivers.docker]
+default_image = "ghcr.io/nvidia/openshell-community/sandboxes/base:latest"
+image_pull_policy = "IfNotPresent"
+sandbox_namespace = "openshell-e2e"
+supervisor_bin = ".cache/openshell-e2e/bin/openshell-sandbox"
diff --git a/e2e/configs/gateway/podman.toml b/e2e/configs/gateway/podman.toml
new file mode 100644
index 0000000000..2ad86099fb
--- /dev/null
+++ b/e2e/configs/gateway/podman.toml
@@ -0,0 +1,29 @@
+# SPDX-FileCopyrightText: Copyright (c) 2025-2026 NVIDIA CORPORATION & AFFILIATES. All rights reserved.
+# SPDX-License-Identifier: Apache-2.0
+
+[openshell]
+version = 1
+
+[openshell.gateway]
+bind_address = "127.0.0.1:8080"
+log_level = "info"
+compute_drivers = ["podman"]
+disable_tls = true
+
+[openshell.gateway.auth]
+allow_unauthenticated_users = true
+
+[openshell.gateway.gateway_jwt]
+signing_key_path = ".cache/openshell-e2e/gateway-jwt/signing.pem"
+public_key_path = ".cache/openshell-e2e/gateway-jwt/public.pem"
+kid_path = ".cache/openshell-e2e/gateway-jwt/kid"
+gateway_id = "openshell-e2e"
+ttl_secs = 0
+
+[openshell.drivers.podman]
+default_image = "ghcr.io/nvidia/openshell-community/sandboxes/base:latest"
+image_pull_policy = "missing"
+network_name = "openshell-e2e"
+grpc_endpoint = "http://10.89.0.1:8080"
+host_gateway_ip = "10.89.0.1"
+supervisor_image = "localhost/openshell/supervisor:e2e-vm"
diff --git a/e2e/run.sh b/e2e/run.sh
new file mode 100755
index 0000000000..eebe38cc54
--- /dev/null
+++ b/e2e/run.sh
@@ -0,0 +1,522 @@
+#!/usr/bin/env bash
+# SPDX-FileCopyrightText: Copyright (c) 2025-2026 NVIDIA CORPORATION & AFFILIATES. All rights reserved.
+# SPDX-License-Identifier: Apache-2.0
+
+# Build the current checkout, run its gateway on the host or in a disposable
+# Nix test guest, and execute one named host-side E2E suite against that gateway.
+
+set -Eeuo pipefail
+
+ROOT="$(cd "$(dirname "${BASH_SOURCE[0]}")/.." && pwd)"
+
+# shellcheck disable=SC1091
+source "${ROOT}/e2e/support/gateway-common.sh"
+# shellcheck disable=SC1091
+source "${ROOT}/tasks/scripts/build-env.sh"
+
+e2e_preserve_mise_dirs
+
+usage() {
+	cat <<'EOF'
+Usage:
+  e2e/run.sh [--vm DISTRO] [--with CONFIG ...] \
+    --gateway-config PATH --suite NAME
+
+Options:
+  --vm DISTRO          Run the gateway in a Nix test guest
+  --with CONFIG        Apply a Nix test-guest configuration; repeatable
+  --gateway-config PATH
+                       Fully resolved gateway TOML
+  --suite NAME         Rust suite at e2e/rust/tests/NAME.rs
+  -h, --help           Show this help
+
+Omit --vm and --with to run the gateway on the host. Supplying --with without
+--vm selects the Ubuntu test guest. Set OPENSHELL_E2E_KEEP=1 to retain state.
+EOF
+}
+
+die() {
+	echo "ERROR: $*" >&2
+	exit 2
+}
+
+require_value() {
+	local option=$1
+	local count=$2
+	local value=${3:-}
+
+	if [ "${count}" -lt 2 ] || [ -z "${value}" ]; then
+		die "${option} requires a value"
+	fi
+	case "${value}" in
+	--*) die "${option} requires a value" ;;
+	esac
+}
+
+resolve_file() {
+	local path=$1
+
+	if [ ! -f "${path}" ]; then
+		return 1
+	fi
+	python3 - "${path}" <<'PY'
+import os
+import sys
+
+print(os.path.realpath(sys.argv[1]))
+PY
+}
+
+catalog_has_entry() {
+	local catalog=$1
+	local section=$2
+	local name=$3
+
+	printf '%s\n' "${catalog}" | awk -v wanted_section="${section}:" -v wanted_name="${name}" '
+		$0 == wanted_section {
+			in_section = 1
+			next
+		}
+		/^[^[:space:]]/ {
+			in_section = 0
+		}
+		in_section && $0 == "  " wanted_name {
+			found = 1
+		}
+		END {
+			exit(found ? 0 : 1)
+		}
+	'
+}
+
+vm=
+gateway_config=
+suite_name=
+with_configurations=()
+
+while [ "$#" -gt 0 ]; do
+	case "$1" in
+	--vm)
+		require_value "$1" "$#" "${2:-}"
+		vm=$2
+		shift 2
+		;;
+	--with)
+		require_value "$1" "$#" "${2:-}"
+		with_configurations+=("$2")
+		shift 2
+		;;
+	--gateway-config)
+		require_value "$1" "$#" "${2:-}"
+		gateway_config=$2
+		shift 2
+		;;
+	--suite)
+		require_value "$1" "$#" "${2:-}"
+		suite_name=$2
+		shift 2
+		;;
+	-h | --help)
+		usage
+		exit 0
+		;;
+	*)
+		die "unknown argument: $1"
+		;;
+	esac
+done
+
+if [ -z "${gateway_config}" ]; then
+	die "--gateway-config is required"
+fi
+if [ -z "${suite_name}" ]; then
+	die "--suite is required"
+fi
+if ! command -v python3 >/dev/null 2>&1; then
+	die "python3 is required"
+fi
+gateway_config_source=${gateway_config}
+if ! gateway_config="$(resolve_file "${gateway_config_source}")"; then
+	die "gateway config does not exist: ${gateway_config_source}"
+fi
+if [[ ! ${suite_name} =~ ^[a-z0-9][a-z0-9-]*$ ]]; then
+	die "suite name must contain only lowercase letters, digits, and hyphens: ${suite_name}"
+fi
+suite_path="${ROOT}/e2e/rust/tests/${suite_name}.rs"
+if [ ! -f "${suite_path}" ]; then
+	die "unknown suite: ${suite_name}"
+fi
+mode=host
+if [ -n "${vm}" ] || [ "${#with_configurations[@]}" -gt 0 ]; then
+	mode=vm
+	if [ -z "${vm}" ]; then
+		vm=ubuntu
+	fi
+fi
+if [ "${mode}" = vm ]; then
+	if [[ ! ${vm} =~ ^[a-z0-9][a-z0-9-]*$ ]]; then
+		die "invalid VM distro name: ${vm}"
+	fi
+	for configuration in "${with_configurations[@]}"; do
+		if [[ ! ${configuration} =~ ^[a-z0-9][a-z0-9-]*$ ]]; then
+			die "invalid VM configuration name: ${configuration}"
+		fi
+	done
+	if ! command -v nix >/dev/null 2>&1; then
+		die "Nix is required for VM mode"
+	fi
+	if ! command -v base64 >/dev/null 2>&1; then
+		die "base64 is required for VM mode"
+	fi
+	if ! vm_catalog="$(cd "${ROOT}" && nix run .#test-guest -- --list)"; then
+		die "failed to read the Nix test-guest catalog"
+	fi
+	if ! catalog_has_entry "${vm_catalog}" Distros "${vm}"; then
+		die "unknown VM distro in the Nix test-guest catalog: ${vm}"
+	fi
+	for configuration in "${with_configurations[@]}"; do
+		if ! catalog_has_entry "${vm_catalog}" Configurations "${configuration}"; then
+			die "unknown VM configuration in the Nix test-guest catalog: ${configuration}"
+		fi
+	done
+fi
+
+gateway_ready_timeout=${OPENSHELL_E2E_GATEWAY_READY_TIMEOUT:-600}
+if [[ ! ${gateway_ready_timeout} =~ ^[1-9][0-9]*$ ]]; then
+	die "OPENSHELL_E2E_GATEWAY_READY_TIMEOUT must be a positive integer"
+fi
+if ! command -v mise >/dev/null 2>&1; then
+	die "mise is required to build OpenShell"
+fi
+if ! command -v openssl >/dev/null 2>&1; then
+	die "OpenSSL is required to generate sandbox JWT keys"
+fi
+
+case "$(uname -m)" in
+x86_64 | amd64)
+	linux_musl_target=x86_64-unknown-linux-musl
+	linux_gateway_rust_target=x86_64-unknown-linux-gnu
+	linux_gateway_zig_target=x86_64-unknown-linux-gnu.2.28
+	;;
+aarch64 | arm64)
+	linux_musl_target=aarch64-unknown-linux-musl
+	linux_gateway_rust_target=aarch64-unknown-linux-gnu
+	linux_gateway_zig_target=aarch64-unknown-linux-gnu.2.28
+	;;
+*)
+	die "unsupported host architecture: $(uname -m)"
+	;;
+esac
+
+cargo_jobs=()
+if [ -n "${CARGO_BUILD_JOBS:-}" ]; then
+	cargo_jobs=(-j "${CARGO_BUILD_JOBS}")
+fi
+
+cd "${ROOT}"
+target_dir="$(e2e_cargo_target_dir "${ROOT}" mise x -- cargo)"
+
+ensure_build_nofile_limit
+
+echo "==> Building native host openshell CLI"
+mise x -- cargo build "${cargo_jobs[@]}" -p openshell-cli --bin openshell
+host_cli_bin="${target_dir}/debug/openshell"
+
+echo "==> Preparing ${linux_musl_target} build target"
+mise x -- rustup target add "${linux_musl_target}" >/dev/null
+
+echo "==> Building Linux openshell-sandbox (${linux_musl_target})"
+mise x -- cargo zigbuild "${cargo_jobs[@]}" \
+	--release \
+	--target "${linux_musl_target}" \
+	-p openshell-sandbox \
+	--bin openshell-sandbox
+linux_sandbox_bin="${target_dir}/${linux_musl_target}/release/openshell-sandbox"
+
+host_gateway_bin=
+guest_gateway_bin=
+if [ "${mode}" = host ]; then
+	echo "==> Building native host openshell-gateway"
+	mise x -- cargo build "${cargo_jobs[@]}" \
+		-p openshell-server \
+		--bin openshell-gateway \
+		--features bundled-z3
+	host_gateway_bin="${target_dir}/debug/openshell-gateway"
+else
+	echo "==> Preparing ${linux_gateway_rust_target} build target"
+	mise x -- rustup target add "${linux_gateway_rust_target}" >/dev/null
+	echo "==> Building Linux openshell-gateway (${linux_gateway_zig_target})"
+	(
+		eval "$(
+			"${ROOT}/tasks/scripts/setup-zig-cc-wrapper.sh" \
+				"${linux_gateway_zig_target}" \
+				"${linux_gateway_zig_target}" \
+				"${target_dir}/zig-gnu-wrapper/e2e"
+		)"
+		mise x -- cargo zigbuild "${cargo_jobs[@]}" \
+			--release \
+			--target "${linux_gateway_zig_target}" \
+			-p openshell-server \
+			--bin openshell-gateway \
+			--features bundled-z3
+	)
+	guest_gateway_bin="${target_dir}/${linux_gateway_rust_target}/release/openshell-gateway"
+fi
+
+expected_binaries=("${host_cli_bin}" "${linux_sandbox_bin}")
+if [ "${mode}" = host ]; then
+	expected_binaries+=("${host_gateway_bin}")
+else
+	expected_binaries+=("${guest_gateway_bin}")
+fi
+for binary in "${expected_binaries[@]}"; do
+	if [ ! -x "${binary}" ]; then
+		echo "ERROR: expected built binary at ${binary}" >&2
+		exit 1
+	fi
+done
+
+run_parent="${ROOT}/.cache/openshell-e2e/runs"
+mkdir -p "${run_parent}"
+run_dir="$(mktemp -d "${run_parent%/}/run.XXXXXX")"
+child_pid=
+runtime_log=
+keep=0
+if [ "${OPENSHELL_E2E_KEEP:-0}" = 1 ]; then
+	keep=1
+fi
+
+start_child() {
+	local working_dir=$1
+	local log_path=$2
+	shift 2
+
+	(
+		cd "${working_dir}"
+		exec python3 -c \
+			'import os, sys; os.setsid(); os.execvp(sys.argv[1], sys.argv[1:])' \
+			"$@"
+	) >"${log_path}" 2>&1 &
+	child_pid=$!
+}
+
+# Invoked by the EXIT trap through cleanup.
+# shellcheck disable=SC2329
+stop_child() {
+	local pid=$1
+	local signal_target="-${pid}"
+
+	if [ -z "${pid}" ] || ! kill -0 "${pid}" 2>/dev/null; then
+		return
+	fi
+	kill -TERM -- "${signal_target}" 2>/dev/null || true
+	for _ in $(seq 1 30); do
+		if ! kill -0 "${pid}" 2>/dev/null; then
+			break
+		fi
+		sleep 1
+	done
+	if kill -0 "${pid}" 2>/dev/null; then
+		kill -KILL -- "${signal_target}" 2>/dev/null || true
+	fi
+	wait "${pid}" 2>/dev/null || true
+}
+
+# Invoked by EXIT, INT, and TERM traps.
+# shellcheck disable=SC2329
+cleanup() {
+	local status=$?
+
+	trap - EXIT INT TERM
+	stop_child "${child_pid}"
+	if [ "${status}" -ne 0 ] && [ -n "${runtime_log}" ] && [ -f "${runtime_log}" ]; then
+		echo "=== ${mode} gateway log ===" >&2
+		cat "${runtime_log}" >&2
+		echo "=== end ${mode} gateway log ===" >&2
+	fi
+	if [ "${keep}" -eq 1 ]; then
+		echo "Kept E2E runner state at ${run_dir}" >&2
+	else
+		rm -rf "${run_dir}"
+	fi
+	exit "${status}"
+}
+
+trap cleanup EXIT
+trap 'exit 130' INT
+trap 'exit 143' TERM
+
+jwt_source_dir="${run_dir}/gateway-jwt"
+host_runtime_dir=
+if [ "${mode}" = host ]; then
+	host_runtime_dir="${run_dir}/host-runtime"
+	jwt_source_dir="${host_runtime_dir}/.cache/openshell-e2e/gateway-jwt"
+fi
+e2e_generate_gateway_jwt "${jwt_source_dir}"
+
+host_port="$(e2e_pick_port)"
+guest_port=
+if [ "${mode}" = vm ]; then
+	guest_port=8080
+fi
+
+export XDG_CONFIG_HOME="${run_dir}/host/config"
+export XDG_DATA_HOME="${run_dir}/host/data"
+export XDG_STATE_HOME="${run_dir}/host/state"
+mkdir -p "${XDG_CONFIG_HOME}" "${XDG_DATA_HOME}" "${XDG_STATE_HOME}"
+
+gateway_name="openshell-e2e-${mode}-${host_port}"
+gateway_endpoint="http://127.0.0.1:${host_port}"
+export OPENSHELL_GATEWAY_ENDPOINT="${gateway_endpoint}"
+export OPENSHELL_GATEWAY="${gateway_name}"
+export OPENSHELL_BIN="${host_cli_bin}"
+
+if [ "${mode}" = host ]; then
+	e2e_align_docker_host_with_cli_context
+	staged_supervisor="${host_runtime_dir}/.cache/openshell-e2e/bin/openshell-sandbox"
+	mkdir -p "$(dirname "${staged_supervisor}")"
+	ln -sfn "${linux_sandbox_bin}" "${staged_supervisor}"
+
+	runtime_log="${run_dir}/gateway.log"
+	echo "==> Starting host gateway at ${gateway_endpoint}"
+	start_child \
+		"${host_runtime_dir}" \
+		"${runtime_log}" \
+		"${host_gateway_bin}" \
+		--config "${gateway_config}" \
+		--bind-address 127.0.0.1 \
+		--port "${host_port}" \
+		--disable-tls
+else
+	runtime_log="${run_dir}/vm.log"
+	guest_launcher="${run_dir}/launch-gateway.sh"
+	guest_launcher_path=/home/openshell/.cache/openshell-e2e/bin/launch-gateway
+	config_payload="$(base64 <"${gateway_config}" | tr -d '\r\n')"
+	jwt_signing_payload="$(base64 <"${jwt_source_dir}/signing.pem" | tr -d '\r\n')"
+	jwt_public_payload="$(base64 <"${jwt_source_dir}/public.pem" | tr -d '\r\n')"
+	jwt_kid_payload="$(base64 <"${jwt_source_dir}/kid" | tr -d '\r\n')"
+	cat >"${guest_launcher}" <<EOF
+#!/usr/bin/env bash
+set -euo pipefail
+
+umask 077
+state_root=/home/openshell/.cache/openshell-e2e
+config_path=\${state_root}/gateway.toml
+jwt_root=\${state_root}/gateway-jwt
+sudo chown -R "\$(id -u):\$(id -g)" /home/openshell/.cache
+chmod 0700 "\${state_root}"
+mkdir -p "\${state_root}/xdg/cache" "\${state_root}/xdg/config" "\${state_root}/xdg/data" "\${state_root}/xdg/state" "\${jwt_root}"
+printf '%s' '${config_payload}' | base64 --decode >"\${config_path}"
+printf '%s' '${jwt_signing_payload}' | base64 --decode >"\${jwt_root}/signing.pem"
+printf '%s' '${jwt_public_payload}' | base64 --decode >"\${jwt_root}/public.pem"
+printf '%s' '${jwt_kid_payload}' | base64 --decode >"\${jwt_root}/kid"
+chmod 0600 "\${config_path}"
+chmod 0600 "\${jwt_root}/signing.pem" "\${jwt_root}/public.pem" "\${jwt_root}/kid"
+export XDG_CONFIG_HOME=\${state_root}/xdg/config
+export XDG_CACHE_HOME=\${state_root}/xdg/cache
+export XDG_DATA_HOME=\${state_root}/xdg/data
+export XDG_STATE_HOME=\${state_root}/xdg/state
+cd /home/openshell
+exec /usr/local/bin/openshell-gateway \
+	--config "\${config_path}" \
+	--bind-address 0.0.0.0 \
+	--port ${guest_port} \
+	--disable-tls
+EOF
+	chmod 0700 "${guest_launcher}"
+
+	vm_args=(
+		nix run .#test-guest --
+		--distro "${vm}"
+	)
+	for configuration in "${with_configurations[@]}"; do
+		vm_args+=(--with "${configuration}")
+	done
+	vm_args+=(
+		--copy "${guest_gateway_bin}:/usr/local/bin/openshell-gateway"
+		--copy "${linux_sandbox_bin}:/home/openshell/.cache/openshell-e2e/bin/openshell-sandbox"
+		--copy "${guest_launcher}:${guest_launcher_path}"
+		--forward-port "${host_port}:${guest_port}"
+	)
+	if [ "${keep}" -eq 1 ]; then
+		vm_args+=(--keep)
+	fi
+	vm_args+=(-- "${guest_launcher_path}")
+
+	echo "==> Starting ${vm} test guest gateway at ${gateway_endpoint}"
+	start_child "${ROOT}" "${runtime_log}" "${vm_args[@]}"
+fi
+
+probe_gateway() {
+	python3 - "${OPENSHELL_BIN}" "${1}" <<'PY'
+import os
+import subprocess
+import sys
+
+with open(sys.argv[2], "wb") as output:
+    try:
+        result = subprocess.run(
+            [sys.argv[1], "status"],
+            env={**os.environ, "NO_COLOR": "1"},
+            stdout=output,
+            stderr=subprocess.STDOUT,
+            timeout=5,
+            check=False,
+        )
+    except subprocess.TimeoutExpired:
+        raise SystemExit(124)
+raise SystemExit(result.returncode)
+PY
+}
+
+wait_for_gateway() {
+	local started_at=${SECONDS}
+	local elapsed=0
+	local process_status
+	local probe_log="${run_dir}/gateway-probe.log"
+
+	echo "==> Waiting up to ${gateway_ready_timeout}s for gateway readiness"
+	while :; do
+		elapsed=$((SECONDS - started_at))
+		if [ "${elapsed}" -ge "${gateway_ready_timeout}" ]; then
+			break
+		fi
+		if ! kill -0 "${child_pid}" 2>/dev/null; then
+			if wait "${child_pid}"; then
+				process_status=0
+			else
+				process_status=$?
+			fi
+			child_pid=
+			echo "ERROR: ${mode} gateway process exited before becoming ready" >&2
+			if [ "${process_status}" -eq 0 ]; then
+				return 1
+			fi
+			return "${process_status}"
+		fi
+		if probe_gateway "${probe_log}" &&
+			grep -q "Connected" "${probe_log}"; then
+			echo "==> Gateway ready after ${elapsed}s"
+			return 0
+		fi
+		sleep 1
+	done
+
+	echo "ERROR: gateway did not become ready within ${gateway_ready_timeout}s" >&2
+	if [ -s "${probe_log}" ]; then
+		echo "=== last gateway probe ===" >&2
+		cat "${probe_log}" >&2
+		echo "=== end last gateway probe ===" >&2
+	fi
+	return 1
+}
+
+wait_for_gateway
+
+echo "==> Running E2E suite: ${suite_name}"
+cd "${ROOT}"
+cargo test \
+	--manifest-path e2e/rust/Cargo.toml \
+	--features e2e \
+	--test "${suite_name}" \
+	-- --nocapture
diff --git a/e2e/support/gateway-common.sh b/e2e/support/gateway-common.sh
index 6b9e6a0956..252cb9a6de 100644
--- a/e2e/support/gateway-common.sh
+++ b/e2e/support/gateway-common.sh
@@ -7,6 +7,12 @@
 
 e2e_cargo_target_dir() {
   local root=$1
+  shift
+  local cargo_command=(cargo)
+
+  if [ "$#" -gt 0 ]; then
+    cargo_command=("$@")
+  fi
 
   if [ -n "${CARGO_TARGET_DIR:-}" ]; then
     case "${CARGO_TARGET_DIR}" in
@@ -16,7 +22,7 @@ e2e_cargo_target_dir() {
     return 0
   fi
 
-  cargo metadata --format-version=1 --no-deps \
+  "${cargo_command[@]}" metadata --format-version=1 --no-deps \
     | python3 -c 'import json, sys; print(json.load(sys.stdin)["target_directory"])'
 }
 
diff --git a/tasks/test.toml b/tasks/test.toml
index 96dde276ce..90e8c6f5e0 100644
--- a/tasks/test.toml
+++ b/tasks/test.toml
@@ -37,6 +37,10 @@ hide = true
 description = "Run all end-to-end tests (Rust + Python + MCP)"
 depends = ["e2e:rust", "e2e:python", "e2e:mcp"]
 
+["e2e:test"]
+description = "Build the current checkout and run a named host or Nix test-guest E2E suite"
+run = "e2e/run.sh"
+
 ["e2e:gpu"]
 description = "Run Docker GPU end-to-end tests"
 depends = ["e2e:docker:gpu"]