diff --git a/docs/releases.rst b/docs/releases.rst
index 63b1d8a2fb..48c188dad5 100644
--- a/docs/releases.rst
+++ b/docs/releases.rst
@@ -36,6 +36,11 @@ contrast to the :ref:`/spec/core/contact` key, this field is not
 supposed to be updated and can be useful when trying to track down
 the original author for consultation.
 
+The ``container`` executor now works in `Fedora Toolbx`__ when Podman is run
+using ``flatpak-spawn --host`` on the host system.
+
+__ https://docs.fedoraproject.org/en-US/fedora-silverblue/toolbox/
+
 
 tmt-1.41.0
 ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
diff --git a/tests/provision/container/toolbox/main.fmf b/tests/provision/container/toolbox/main.fmf
new file mode 100644
index 0000000000..5dc7b4f4f4
--- /dev/null
+++ b/tests/provision/container/toolbox/main.fmf
@@ -0,0 +1,24 @@
+summary: Test container provisioner in toolbox
+description:
+    Verify that container provisioner works well when tmt is run from
+    a toolbox container and podman is run on the host system using
+    `flatpak-spawn --host`. This is a common setup used in Fedora
+    Silverblue.
+
+require:
+    - toolbox
+tag+:
+  - provision-only
+  - provision-container
+require+:
+  - toolbox
+adjust+:
+  - enabled: false
+    when: distro != fedora
+    because: Setting up toolbox on CS9 with default UBI9 toolbox image is a pain.
+  - check:
+      - how: avc
+        result: xfail
+    when: distro >= fedora-41
+    because: |
+      We are not interested in AVCs for this test due to complicated setup.
diff --git a/tests/provision/container/toolbox/podman_wrapper b/tests/provision/container/toolbox/podman_wrapper
new file mode 100755
index 0000000000..a1792117bf
--- /dev/null
+++ b/tests/provision/container/toolbox/podman_wrapper
@@ -0,0 +1,2 @@
+#!/bin/bash
+flatpak-spawn --host podman "$@"
diff --git a/tests/provision/container/toolbox/test.sh b/tests/provision/container/toolbox/test.sh
new file mode 100755
index 0000000000..a1d7e3a452
--- /dev/null
+++ b/tests/provision/container/toolbox/test.sh
@@ -0,0 +1,84 @@
+#!/bin/bash
+. /usr/share/beakerlib/beakerlib.sh || exit 1
+
+# Use `tmt try` to run this test locally, running directly the script will not work.
+
+rlJournalStart
+    rlPhaseStartSetup
+        rlRun "toolbox_container_name=\$(uuidgen)" 0 "Generate toolbox container name"
+        rlRun "toolbox_user=toolbox" 0 "Set user for running toolbox"
+    rlPhaseEnd
+
+    rlPhaseStartTest "Create toolbox container"
+        # Add a toolbox user. Running toolbox under root user does not work well,
+        # so a separate user account is created.
+        rlRun "useradd $toolbox_user"
+        rlRun "toolbox_user_id=$(id -u $toolbox_user)"
+
+        # Make sure systemd user session runs for the new user. The user session
+        # hosts a dbus session, which is required for toolbox.
+        rlRun "loginctl enable-linger $toolbox_user"
+
+        # Add required environment variables for toolbox to the user's environment.
+        rlRun "echo export XDG_RUNTIME_DIR=/run/user/$toolbox_user_id >> /home/$toolbox_user/.bashrc"
+        rlRun "echo export DBUS_SESSION_BUS_ADDRESS=unix:path=/run/user/$toolbox_user_id/bus >> /home/$toolbox_user/.bashrc"
+
+        rlRun "sudo -iu $toolbox_user toolbox create -y $toolbox_container_name"
+    rlPhaseEnd
+
+    toolbox_run() {
+        local command="sudo -iu $toolbox_user toolbox run --container $toolbox_container_name $*"
+        echo "Command: $command"
+        eval "$command"
+    }
+
+    rlPhaseStartTest "Local execution via tmt: Install tmt from TMT_TREE"
+        TOOLBOX_TREE="/var/tmp/tree"
+        TMT_COMMAND="env -C ${TOOLBOX_TREE} hatch -e dev run env -C /tmp tmt"
+
+        rlRun "type toolbox_run"
+
+        # Install make and hatch
+        rlRun "toolbox_run sudo dnf -y install make hatch"
+
+        # Create a copy of the tmt tree, to mitigate possible permission issues
+        rlRun "cp -Rf ${TMT_TREE} ${TOOLBOX_TREE}"
+
+        # Copy tmt project into the toolbox container
+        rlRun "sudo -iu ${toolbox_user} podman cp ${TOOLBOX_TREE} $toolbox_container_name:${TOOLBOX_TREE}"
+
+        # Fix permissions for the toolbox user
+        rlRun "toolbox_run sudo chown -Rf ${toolbox_user}:${toolbox_user} ${TOOLBOX_TREE}"
+
+        # Initialize git in tmt tree, it is required for development installation
+        # and the tmt tree is not a git repository.
+        rlRun "toolbox_run git -C ${TOOLBOX_TREE} init"
+
+        # Install additional development dependencies
+        rlRun "toolbox_run make -C ${TOOLBOX_TREE} develop"
+    rlPhaseEnd
+
+    rlPhaseStartTest "Print tmt version installed in toolbox"
+        rlRun "toolbox_run $TMT_COMMAND --version"
+    rlPhaseEnd
+
+    rlPhaseStartTest "Add podman wrapper"
+        # Copy the wrapper from the toolbox user, the containers are local to the user.
+        # Need to use a copy of the wrapper, the TMT_TREE is a volume mount and thus
+        # it is not accessible to the toolbox user.
+        rlRun "cp podman_wrapper /tmp/podman_wrapper"
+        rlRun "sudo -iu ${toolbox_user} podman cp /tmp/podman_wrapper $toolbox_container_name:/usr/bin/podman"
+        rlRun "toolbox_run podman --version"
+    rlPhaseEnd
+
+    rlPhaseStartTest "Verify container provisioner works from toolbox"
+        rlRun RUNID="$(mktemp -u)"
+        rlRun -s "toolbox_run env -C /tmp ${TMT_COMMAND} run -i ${RUNID} -a -vvv provision -h container -i registry.fedoraproject.org/fedora:latest execute -h tmt -s \\\"echo hello from container\\\""
+        rlAssertGrep "content: hello from container" $rlRun_LOG
+    rlPhaseEnd
+
+    rlPhaseStartCleanup
+        rlRun "toolbox rm -f $toolbox_container_name" 0 "Remove toolbox container"
+        rlRun "userdel -rf toolbox"
+    rlPhaseEnd
+rlJournalEnd
diff --git a/tmt/steps/provision/__init__.py b/tmt/steps/provision/__init__.py
index 1c04d4c556..2499382bfc 100644
--- a/tmt/steps/provision/__init__.py
+++ b/tmt/steps/provision/__init__.py
@@ -329,6 +329,8 @@ class GuestFacts(SerializableContainer):
     has_selinux: Optional[bool] = None
     is_superuser: Optional[bool] = None
     is_ostree: Optional[bool] = None
+    is_toolbox: Optional[bool] = None
+    toolbox_container_name: Optional[str] = None
 
     #: Various Linux capabilities and whether they are permitted to
     #: commands executed on this guest.
@@ -589,6 +591,47 @@ def _query_is_ostree(self, guest: 'Guest') -> Optional[bool]:
 
         return output.stdout.strip() == 'yes'
 
+    def _query_is_toolbox(self, guest: 'Guest') -> Optional[bool]:
+        # https://www.reddit.com/r/Fedora/comments/g6flgd/toolbox_specific_environment_variables/
+        output = self._execute(
+            guest,
+            Command(
+                tmt.utils.DEFAULT_SHELL,
+                '-c',
+                'if [ -e /run/.toolboxenv ]; then echo yes; else echo no; fi'))
+
+        if output is None or output.stdout is None:
+            return None
+
+        return output.stdout.strip() == 'yes'
+
+    def _query_toolbox_container_name(self, guest: 'Guest') -> Optional[str]:
+        output = self._execute(
+            guest,
+            Command(
+                tmt.utils.DEFAULT_SHELL,
+                '-c',
+                'if [ -e /run/.containerenv ]; then echo yes; else echo no; fi'))
+
+        if output is None or output.stdout is None:
+            return None
+
+        if output.stdout.strip() == 'no':
+            return None
+
+        output = self._execute(
+            guest,
+            Command('cat', '/run/.containerenv'))
+
+        if output is None or output.stdout is None:
+            return None
+
+        for line in output.stdout.splitlines():
+            if line.startswith('name="'):
+                return line[6:-1]
+
+        return None
+
     def _query_capabilities(self, guest: 'Guest') -> dict[GuestCapability, bool]:
         # TODO: there must be a canonical way of getting permitted capabilities.
         # For now, we're interested in whether we can access kernel message buffer.
@@ -610,6 +653,8 @@ def sync(self, guest: 'Guest') -> None:
         self.has_selinux = self._query_has_selinux(guest)
         self.is_superuser = self._query_is_superuser(guest)
         self.is_ostree = self._query_is_ostree(guest)
+        self.is_toolbox = self._query_is_toolbox(guest)
+        self.toolbox_container_name = self._query_toolbox_container_name(guest)
         self.capabilities = self._query_capabilities(guest)
 
         self.in_sync = True
diff --git a/tmt/steps/provision/podman.py b/tmt/steps/provision/podman.py
index f5021e570d..92514d4ed4 100644
--- a/tmt/steps/provision/podman.py
+++ b/tmt/steps/provision/podman.py
@@ -383,10 +383,22 @@ def push(
             self._run_guest_command(Command(
                 "chcon", "--recursive", "--type=container_file_t", self.parent.plan.workdir
                 ), shell=False, silent=True)
+
         # In case explicit destination is given, use `podman cp` to copy data
-        # to the container
+        # to the container. If running in toolbox, make sure to copy from the toolbox
+        # container instead of localhost.
         if source and destination:
-            self.podman(Command("cp", source, f"{self.container}:{destination}"))
+            container_name: Optional[str] = None
+            if self.parent.plan.my_run.runner.facts.is_toolbox:
+                container_name = self.parent.plan.my_run.runner.facts.toolbox_container_name
+            self.podman(
+                Command(
+                    "cp",
+                    f"{container_name}:{source}"
+                    if container_name else source,
+                    f"{self.container}:{destination}"
+                    )
+                )
 
     def pull(
             self,