diff --git a/.github/workflows/ci.yml b/.github/workflows/ci.yml
index 27f60574e0c..cb97fd211dd 100644
--- a/.github/workflows/ci.yml
+++ b/.github/workflows/ci.yml
@@ -128,7 +128,7 @@ jobs:
     - run: exec bash -c "nix-channel --update && nix-env -iA nixpkgs.hello && hello"
 
   docker_push_image:
-    needs: [check_secrets, tests]
+    needs: [check_secrets, tests, vm_tests]
     permissions:
       contents: read
       packages: write
@@ -194,7 +194,13 @@ jobs:
       - uses: actions/checkout@v4
       - uses: DeterminateSystems/nix-installer-action@main
       - uses: DeterminateSystems/magic-nix-cache-action@main
-      - run: nix build -L .#hydraJobs.tests.githubFlakes .#hydraJobs.tests.tarballFlakes .#hydraJobs.tests.functional_user
+      - run: |
+          nix build -L \
+            .#hydraJobs.tests.functional_user \
+            .#hydraJobs.tests.githubFlakes \
+            .#hydraJobs.tests.nix-docker \
+            .#hydraJobs.tests.tarballFlakes \
+            ;
 
   flake_regressions:
     needs: vm_tests
diff --git a/doc/manual/source/installation/installing-docker.md b/doc/manual/source/installation/installing-docker.md
index 6f77d6a5708..9354c1a7228 100644
--- a/doc/manual/source/installation/installing-docker.md
+++ b/doc/manual/source/installation/installing-docker.md
@@ -57,3 +57,21 @@ $ nix build ./\#hydraJobs.dockerImage.x86_64-linux
 $ docker load -i ./result/image.tar.gz
 $ docker run -ti nix:2.5pre20211105
 ```
+
+# Docker image with non-root Nix
+
+If you would like to run Nix in a container under a user other than `root`,
+you can build an image with a non-root single-user installation of Nix
+by specifying the `uid`, `gid`, `uname`, and `gname` arguments to `docker.nix`:
+
+```console
+$ nix build --file docker.nix \
+    --arg uid 1000 \
+    --arg gid 1000 \
+    --argstr uname user \
+    --argstr gname user \
+    --argstr name nix-user \
+    --out-link nix-user.tar.gz
+$ docker load -i nix-user.tar.gz
+$ docker run -ti nix-user
+```
diff --git a/docker.nix b/docker.nix
index bd16b71cd71..19479e57c18 100644
--- a/docker.nix
+++ b/docker.nix
@@ -9,6 +9,10 @@
 , maxLayers ? 100
 , nixConf ? {}
 , flake-registry ? null
+, uid ? 0
+, gid ? 0
+, uname ? "root"
+, gname ? "root"
 }:
 let
   defaultPkgs = with pkgs; [
@@ -50,6 +54,15 @@ let
       description = "Unprivileged account (don't use!)";
     };
 
+  } // lib.optionalAttrs (uid != 0) {
+    "${uname}" = {
+      uid = uid;
+      shell = "${pkgs.bashInteractive}/bin/bash";
+      home = "/home/${uname}";
+      gid = gid;
+      groups = [ "${gname}" ];
+      description = "Nix user";
+    };
   } // lib.listToAttrs (
     map
       (
@@ -70,6 +83,8 @@ let
     root.gid = 0;
     nixbld.gid = 30000;
     nobody.gid = 65534;
+  } // lib.optionalAttrs (gid != 0) {
+    "${gname}".gid = gid;
   };
 
   userToPasswd = (
@@ -150,6 +165,8 @@ let
     in
       "${n} = ${vStr}") (defaultNixConf // nixConf))) + "\n";
 
+  userHome = if uid == 0 then "/root" else "/home/${uname}";
+
   baseSystem =
     let
       nixpkgs = pkgs.path;
@@ -237,26 +254,26 @@ let
       mkdir -p $out/etc/nix
       cat $nixConfContentsPath > $out/etc/nix/nix.conf
 
-      mkdir -p $out/root
-      mkdir -p $out/nix/var/nix/profiles/per-user/root
+      mkdir -p $out${userHome}
+      mkdir -p $out/nix/var/nix/profiles/per-user/${uname}
 
       ln -s ${profile} $out/nix/var/nix/profiles/default-1-link
       ln -s $out/nix/var/nix/profiles/default-1-link $out/nix/var/nix/profiles/default
-      ln -s /nix/var/nix/profiles/default $out/root/.nix-profile
+      ln -s /nix/var/nix/profiles/default $out${userHome}/.nix-profile
 
-      ln -s ${channel} $out/nix/var/nix/profiles/per-user/root/channels-1-link
-      ln -s $out/nix/var/nix/profiles/per-user/root/channels-1-link $out/nix/var/nix/profiles/per-user/root/channels
+      ln -s ${channel} $out/nix/var/nix/profiles/per-user/${uname}/channels-1-link
+      ln -s $out/nix/var/nix/profiles/per-user/${uname}/channels-1-link $out/nix/var/nix/profiles/per-user/${uname}/channels
 
-      mkdir -p $out/root/.nix-defexpr
-      ln -s $out/nix/var/nix/profiles/per-user/root/channels $out/root/.nix-defexpr/channels
-      echo "${channelURL} ${channelName}" > $out/root/.nix-channels
+      mkdir -p $out${userHome}/.nix-defexpr
+      ln -s $out/nix/var/nix/profiles/per-user/${uname}/channels $out${userHome}/.nix-defexpr/channels
+      echo "${channelURL} ${channelName}" > $out${userHome}/.nix-channels
 
       mkdir -p $out/bin $out/usr/bin
       ln -s ${pkgs.coreutils}/bin/env $out/usr/bin/env
       ln -s ${pkgs.bashInteractive}/bin/bash $out/bin/sh
 
     '' + (lib.optionalString (flake-registry-path != null) ''
-      nixCacheDir="/root/.cache/nix"
+      nixCacheDir="${userHome}/.cache/nix"
       mkdir -p $out$nixCacheDir
       globalFlakeRegistryPath="$nixCacheDir/flake-registry.json"
       ln -s ${flake-registry-path} $out$globalFlakeRegistryPath
@@ -268,7 +285,7 @@ let
 in
 pkgs.dockerTools.buildLayeredImageWithNixDb {
 
-  inherit name tag maxLayers;
+  inherit name tag maxLayers uid gid uname gname;
 
   contents = [ baseSystem ];
 
@@ -279,25 +296,28 @@ pkgs.dockerTools.buildLayeredImageWithNixDb {
   fakeRootCommands = ''
     chmod 1777 tmp
     chmod 1777 var/tmp
+    chown -R ${toString uid}:${toString gid} .${userHome}
+    chown -R ${toString uid}:${toString gid} nix
   '';
 
   config = {
-    Cmd = [ "/root/.nix-profile/bin/bash" ];
+    Cmd = [ "${userHome}/.nix-profile/bin/bash" ];
+    User = "${toString uid}:${toString gid}";
     Env = [
-      "USER=root"
+      "USER=${uname}"
       "PATH=${lib.concatStringsSep ":" [
-        "/root/.nix-profile/bin"
+        "${userHome}/.nix-profile/bin"
         "/nix/var/nix/profiles/default/bin"
         "/nix/var/nix/profiles/default/sbin"
       ]}"
       "MANPATH=${lib.concatStringsSep ":" [
-        "/root/.nix-profile/share/man"
+        "${userHome}/.nix-profile/share/man"
         "/nix/var/nix/profiles/default/share/man"
       ]}"
       "SSL_CERT_FILE=/nix/var/nix/profiles/default/etc/ssl/certs/ca-bundle.crt"
       "GIT_SSL_CAINFO=/nix/var/nix/profiles/default/etc/ssl/certs/ca-bundle.crt"
       "NIX_SSL_CERT_FILE=/nix/var/nix/profiles/default/etc/ssl/certs/ca-bundle.crt"
-      "NIX_PATH=/nix/var/nix/profiles/per-user/root/channels:/root/.nix-defexpr/channels"
+      "NIX_PATH=/nix/var/nix/profiles/per-user/${uname}/channels:${userHome}/.nix-defexpr/channels"
     ];
   };
 
diff --git a/tests/nixos/default.nix b/tests/nixos/default.nix
index 17bfdea3822..c5f4a23aa08 100644
--- a/tests/nixos/default.nix
+++ b/tests/nixos/default.nix
@@ -124,6 +124,8 @@ in
 
   nix-copy = runNixOSTestFor "x86_64-linux" ./nix-copy.nix;
 
+  nix-docker = runNixOSTestFor "x86_64-linux" ./nix-docker.nix;
+
   nssPreload = runNixOSTestFor "x86_64-linux" ./nss-preload.nix;
 
   githubFlakes = runNixOSTestFor "x86_64-linux" ./github-flakes.nix;
diff --git a/tests/nixos/nix-docker-test.sh b/tests/nixos/nix-docker-test.sh
new file mode 100644
index 00000000000..1f65e1a9446
--- /dev/null
+++ b/tests/nixos/nix-docker-test.sh
@@ -0,0 +1,47 @@
+#!/usr/bin/env bash
+# docker.nix test script. Runs inside a built docker.nix container.
+
+set -eEuo pipefail
+
+export NIX_CONFIG='substituters = http://cache:5000?trusted=1'
+
+cd /tmp
+
+# Test getting a fetched derivation
+test "$("$(nix-build -E '(import <nixpkgs> {}).hello')"/bin/hello)" = "Hello, world!"
+
+# Test building a simple derivation
+# shellcheck disable=SC2016
+nix-build -E '
+let
+  pkgs = import <nixpkgs> {};
+in
+builtins.derivation {
+  name = "test";
+  system = builtins.currentSystem;
+  builder = "${pkgs.bash}/bin/bash";
+  args = ["-c" "echo OK > $out"];
+}'
+test "$(cat result)" = OK
+
+# Ensure #!/bin/sh shebang works
+echo '#!/bin/sh' > ./shebang-test
+echo 'echo OK' >> ./shebang-test
+chmod +x ./shebang-test
+test "$(./shebang-test)" = OK
+
+# Ensure #!/usr/bin/env shebang works
+echo '#!/usr/bin/env bash' > ./shebang-test
+echo 'echo OK' >> ./shebang-test
+chmod +x ./shebang-test
+test "$(./shebang-test)" = OK
+
+# Test nix-shell
+{
+    echo '#!/usr/bin/env nix-shell'
+    echo '#! nix-shell -i bash'
+    echo '#! nix-shell -p hello'
+    echo 'hello'
+} > ./nix-shell-test
+chmod +x ./nix-shell-test
+test "$(./nix-shell-test)" = "Hello, world!"
diff --git a/tests/nixos/nix-docker.nix b/tests/nixos/nix-docker.nix
new file mode 100644
index 00000000000..dfd50898894
--- /dev/null
+++ b/tests/nixos/nix-docker.nix
@@ -0,0 +1,53 @@
+# Test the container built by ../../docker.nix.
+
+{ lib, config, nixpkgs, hostPkgs, ... }:
+
+let
+  pkgs = config.nodes.machine.nixpkgs.pkgs;
+
+  nixImage = import ../../docker.nix {
+    inherit (config.nodes.machine.nixpkgs) pkgs;
+  };
+  nixUserImage = import ../../docker.nix {
+    inherit (config.nodes.machine.nixpkgs) pkgs;
+    name = "nix-user";
+    uid = 1000;
+    gid = 1000;
+    uname = "user";
+    gname = "user";
+  };
+
+  containerTestScript = ./nix-docker-test.sh;
+
+in {
+  name = "nix-docker";
+
+  nodes =
+    { machine =
+        { config, lib, pkgs, ... }:
+        { virtualisation.diskSize = 4096;
+        };
+      cache =
+        { config, lib, pkgs, ... }:
+        { virtualisation.additionalPaths = [ pkgs.stdenv pkgs.hello ];
+          services.harmonia.enable = true;
+          networking.firewall.allowedTCPPorts = [ 5000 ];
+        };
+    };
+
+  testScript = { nodes }: ''
+    cache.wait_for_unit("harmonia.service")
+
+    machine.succeed("mkdir -p /etc/containers")
+    machine.succeed("""echo '{"default":[{"type":"insecureAcceptAnything"}]}' > /etc/containers/policy.json""")
+
+    machine.succeed("${pkgs.podman}/bin/podman load -i ${nixImage}")
+    machine.succeed("${pkgs.podman}/bin/podman run --rm nix nix --version")
+    machine.succeed("${pkgs.podman}/bin/podman run --rm -i nix < ${containerTestScript}")
+
+    machine.succeed("${pkgs.podman}/bin/podman load -i ${nixUserImage}")
+    machine.succeed("${pkgs.podman}/bin/podman run --rm nix-user nix --version")
+    machine.succeed("${pkgs.podman}/bin/podman run --rm -i nix-user < ${containerTestScript}")
+    machine.succeed("[[ $(${pkgs.podman}/bin/podman run --rm nix-user stat -c %u /nix/store) = 1000 ]]")
+  '';
+}