diff --git a/src/cmd/run.go b/src/cmd/run.go
index 7db7d9ef7..d243a343e 100644
--- a/src/cmd/run.go
+++ b/src/cmd/run.go
@@ -298,6 +298,7 @@ func runCommandWithFallbacks(container string, command []string, emitEscapeSeque
 	runFallbackCommandsIndex := 0
 	runFallbackWorkDirsIndex := 0
 	workDir := workingDirectory
+	runFallbackWorkDirs := append([]string{"/run/host" + workDir}, runFallbackWorkDirs...)
 
 	for {
 		execArgs := constructExecArgs(container, command, detachKeysSupported, envOptions, workDir)
@@ -522,7 +523,7 @@ func isPathPresent(container, path string) (bool, error) {
 		"exec",
 		"--user", currentUser.Username,
 		container,
-		"sh", "-c", "test -d \"$1\"", "sh", path,
+		"sh", "-c", "test -d \"$1\" -a \"$1\" -ef \"/run/host/$1\"", "sh", path,
 	}
 
 	if err := shell.Run("podman", nil, nil, nil, args...); err != nil {
diff --git a/test/system/104-run.bats b/test/system/104-run.bats
index 5bb92f8e3..f2e989565 100644
--- a/test/system/104-run.bats
+++ b/test/system/104-run.bats
@@ -1,4 +1,19 @@
 #!/usr/bin/env bats
+#
+# Copyright © 2021 – 2022 Red Hat, Inc.
+#
+# Licensed under the Apache License, Version 2.0 (the "License");
+# you may not use this file except in compliance with the License.
+# You may obtain a copy of the License at
+#
+#     http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing, software
+# distributed under the License is distributed on an "AS IS" BASIS,
+# WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+# See the License for the specific language governing permissions and
+# limitations under the License.
+#
 
 load 'libs/bats-support/load'
 load 'libs/bats-assert/load'
@@ -13,98 +28,283 @@ teardown() {
   cleanup_containers
 }
 
-@test "run: Try to run a command in the default container with no containers created" {
-  local default_container_name="$(get_system_id)-toolbox-$(get_system_version)"
+@test "run: Smoke test with true(1)" {
+  create_default_container
 
   run $TOOLBOX run true
 
+  assert_success
+  assert_output ""
+}
+
+@test "run: Smoke test with false(1)" {
+  create_default_container
+
+  run -1 $TOOLBOX run false
+
   assert_failure
+  assert_output ""
+}
+
+@test "run: Ensure that a login shell is used to invoke the command" {
+  create_default_container
+
+  cp "$HOME"/.bash_profile "$HOME"/.bash_profile.orig
+  echo "echo \"~/.bash_profile read\"" >>"$HOME"/.bash_profile
+
+  run $TOOLBOX run true
+
+  mv "$HOME"/.bash_profile.orig "$HOME"/.bash_profile
+
+  assert_success
+  assert_line --index 0 "~/.bash_profile read"
+  assert [ ${#lines[@]} -eq 1 ]
+}
+
+@test "run: 'echo \"Hello World\"' inside the default container" {
+  create_default_container
+
+  run $TOOLBOX --verbose run echo "Hello World"
+
+  assert_success
+  assert_line --index $((${#lines[@]}-1)) "Hello World"
+}
+
+@test "run: 'echo \"Hello World\"' inside a restarted container" {
+  create_container running
+
+  start_container running
+  stop_container running
+
+  run $TOOLBOX --verbose run --container running echo "Hello World"
+
+  assert_success
+  assert_line --index $((${#lines[@]}-1)) "Hello World"
+}
+
+@test "run: 'sudo id' inside the default container" {
+  create_default_container
+
+  output="$($TOOLBOX --verbose run sudo id 2>$BATS_TMPDIR/stderr)"
+  status="$?"
+
+  echo "# stderr"
+  cat $BATS_TMPDIR/stderr
+  echo "# stdout"
+  echo $output
+
+  assert_success
+  assert_output --partial "uid=0(root)"
+}
+
+@test "run: Ensure that /run/.containerenv exists" {
+  create_default_container
+
+  run --separate-stderr $TOOLBOX run cat /run/.containerenv
+
+  assert_success
+  assert [ ${#lines[@]} -gt 0 ]
+  assert [ ${#stderr_lines[@]} -eq 0 ]
+}
+
+@test "run: Ensure that /run/.toolboxenv exists" {
+  create_default_container
+
+  run --separate-stderr $TOOLBOX run test -f /run/.toolboxenv
+
+  assert_success
+  assert [ ${#lines[@]} -eq 0 ]
+  assert [ ${#stderr_lines[@]} -eq 0 ]
+}
+
+@test "run: Ensure that the default container is used" {
+  run echo "$name"
+
+  assert_success
+  assert_output ""
+
+  local default_container_name="$(get_system_id)-toolbox-$(get_system_version)"
+  create_default_container
+  create_container other-container
+
+  run --separate-stderr $TOOLBOX run cat /run/.containerenv
+
+  assert_success
+  assert [ ${#lines[@]} -gt 0 ]
+  assert [ ${#stderr_lines[@]} -eq 0 ]
+
+  source <(echo "$output")
+  run echo "$name"
+
+  assert_success
+  assert_output "$default_container_name"
+}
+
+@test "run: Ensure that a specific container is used" {
+  run echo "$name"
+
+  assert_success
+  assert_output ""
+
+  local default_container_name="$(get_system_id)-toolbox-$(get_system_version)"
+  create_default_container
+  create_container other-container
+
+  run --separate-stderr $TOOLBOX run --container other-container cat /run/.containerenv
+
+  assert_success
+  assert [ ${#lines[@]} -gt 0 ]
+  assert [ ${#stderr_lines[@]} -eq 0 ]
+
+  source <(echo "$output")
+  run echo "$name"
+
+  assert_success
+  assert_output "other-container"
+}
+
+@test "run: Ensure that /run/host is used as a fallback working directory" {
+  local default_container_name="$(get_system_id)-toolbox-$(get_system_version)"
+  create_default_container
+
+  pushd /etc/kernel
+  run --separate-stderr $TOOLBOX run pwd
+  popd
+
+  assert_success
+  assert_line --index 0 "/run/host/etc/kernel"
+  assert [ ${#lines[@]} -eq 1 ]
+  lines=("${stderr_lines[@]}")
+  assert_line --index $((${#stderr_lines[@]}-2)) "Error: directory /etc/kernel not found in container $default_container_name"
+  assert_line --index $((${#stderr_lines[@]}-1)) "Using /run/host/etc/kernel instead."
+  assert [ ${#stderr_lines[@]} -gt 2 ]
+}
+
+@test "run: Pass down 1 additional file descriptor" {
+  create_default_container
+
+  # File descriptors 3 and 4 are reserved by Bats.
+  run --separate-stderr $TOOLBOX run --preserve-fds 3 readlink /proc/self/fd/5 5>/dev/null
+
+  assert_success
+  assert_line --index 0 "/dev/null"
+  assert [ ${#lines[@]} -eq 1 ]
+  assert [ ${#stderr_lines[@]} -eq 0 ]
+}
+
+@test "run: Try the non-existent default container with none other present" {
+  local default_container_name="$(get_system_id)-toolbox-$(get_system_version)"
+
+  run --separate-stderr $TOOLBOX run true
+
+  assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: container $default_container_name not found"
   assert_line --index 1 "Use the 'create' command to create a toolbox."
   assert_line --index 2 "Run 'toolbox --help' for usage."
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Try to run a command in the default container when 1 non-default container is present" {
+@test "run: Try the non-existent default container with another present" {
   local default_container_name="$(get_system_id)-toolbox-$(get_system_version)"
 
   create_container other-container
 
-  run $TOOLBOX run true
+  run --separate-stderr $TOOLBOX run true
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: container $default_container_name not found"
   assert_line --index 1 "Use the 'create' command to create a toolbox."
   assert_line --index 2 "Run 'toolbox --help' for usage."
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Try to run a command in a specific non-existent container" {
+@test "run: Try a specific non-existent container with another present" {
   create_container other-container
 
-  run $TOOLBOX run -c wrong-container true
+  run --separate-stderr $TOOLBOX run --container wrong-container true
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: container wrong-container not found"
   assert_line --index 1 "Use the 'create' command to create a toolbox."
   assert_line --index 2 "Run 'toolbox --help' for usage."
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Try to run a command in a container based on unsupported distribution" {
+@test "run: Try an unsupported distribution" {
   local distro="foo"
 
-  run $TOOLBOX --assumeyes run --distro "$distro" ls
+  run --separate-stderr $TOOLBOX --assumeyes run --distro "$distro" ls
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: invalid argument for '--distro'"
   assert_line --index 1 "Distribution $distro is unsupported."
   assert_line --index 2 "Run 'toolbox --help' for usage."
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Try to run a command in a container based on Fedora but with wrong version" {
-  run $TOOLBOX run -d fedora -r foobar ls
+@test "run: Try Fedora with an invalid release" {
+  run --separate-stderr $TOOLBOX run --distro fedora --release foobar ls
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: invalid argument for '--release'"
   assert_line --index 1 "The release must be a positive integer."
   assert_line --index 2 "Run 'toolbox --help' for usage."
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 
-  run $TOOLBOX run --distro fedora --release -3 ls
+  run --separate-stderr $TOOLBOX run --distro fedora --release -3 ls
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: invalid argument for '--release'"
   assert_line --index 1 "The release must be a positive integer."
   assert_line --index 2 "Run 'toolbox --help' for usage."
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Try to run a command in a container based on RHEL but with wrong version" {
-  run $TOOLBOX run --distro rhel --release 8 ls
+@test "run: Try RHEL with an invalid release" {
+  run --separate-stderr $TOOLBOX run --distro rhel --release 8 ls
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: invalid argument for '--release'"
   assert_line --index 1 "The release must be in the '<major>.<minor>' format."
   assert_line --index 2 "Run 'toolbox --help' for usage."
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 
-  run $TOOLBOX run --distro rhel --release 8.2foo ls
+  run --separate-stderr $TOOLBOX run --distro rhel --release 8.2foo ls
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: invalid argument for '--release'"
   assert_line --index 1 "The release must be in the '<major>.<minor>' format."
   assert_line --index 2 "Run 'toolbox --help' for usage."
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 
-  run $TOOLBOX run --distro rhel --release -2.1 ls
+  run --separate-stderr $TOOLBOX run --distro rhel --release -2.1 ls
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: invalid argument for '--release'"
   assert_line --index 1 "The release must be a positive number."
   assert_line --index 2 "Run 'toolbox --help' for usage."
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Try to run a command in a container based on non-default distro without providing a version" {
+@test "run: Try a non-default distro without a release" {
   local distro="fedora"
   local system_id="$(get_system_id)"
 
@@ -112,92 +312,65 @@ teardown() {
     distro="rhel"
   fi
 
-  run $TOOLBOX run -d "$distro" ls
+  run --separate-stderr $TOOLBOX run --distro "$distro" ls
 
   assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
   assert_line --index 0 "Error: option '--release' is needed"
   assert_line --index 1 "Distribution $distro doesn't match the host."
   assert_line --index 2 "Run 'toolbox --help' for usage."
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Run echo 'Hello World' inside of the default container" {
+@test "run: Smoke test with 'exit 2'" {
   create_default_container
 
-  run $TOOLBOX --verbose run echo -n "Hello World"
-
-  assert_success
-  assert_line --index $((${#lines[@]}-1)) "Hello World"
-}
-
-@test "run: Run echo 'Hello World' inside a container after being stopped" {
-  create_container running
-
-  start_container running
-  stop_container running
-
-  run $TOOLBOX --verbose run --container running echo -n "Hello World"
-
-  assert_success
-  assert_line --index $((${#lines[@]}-1)) "Hello World"
+  run -2 $TOOLBOX run /bin/sh -c 'exit 2'
+  assert_failure
+  assert_output ""
 }
 
-@test "run: Run sudo id inside of the default container" {
+@test "run: Pass down 1 invalid file descriptor" {
+  local default_container_name="$(get_system_id)-toolbox-$(get_system_version)"
   create_default_container
 
-  output="$($TOOLBOX --verbose run sudo id 2>$BATS_TMPDIR/stderr)"
-  status="$?"
-
-  echo "# stderr"
-  cat $BATS_TMPDIR/stderr
-  echo "# stdout"
-  echo $output
+  # File descriptors 3 and 4 are reserved by Bats.
+  run -125 --separate-stderr $TOOLBOX run --preserve-fds 3 readlink /proc/self/fd/5
 
-  assert_success
-  assert_output --partial "uid=0(root)"
+  assert_failure
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
+  assert_line --index 0 "Error: file descriptor 5 is not available - the preserve-fds option requires that file descriptors must be passed"
+  assert_line --index 1 "Error: failed to invoke 'podman exec' in container $default_container_name"
+  assert [ ${#stderr_lines[@]} -eq 2 ]
 }
 
-@test "run: Run command exiting with zero code in the default container" {
+@test "run: Try /etc as a command" {
   create_default_container
 
-  run $TOOLBOX run /bin/sh -c 'exit 0'
-
-  assert_success
-  assert_output ""
-}
-
-@test "run: Run command exiting with non-zero code in the default container" {
-  create_default_container
+  run -126 --separate-stderr $TOOLBOX run /etc
 
-  run $TOOLBOX run /bin/sh -c 'exit 2'
   assert_failure
-  assert [ $status -eq 2 ]
-  assert_output ""
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
+  assert_line --index 0 "bash: line 1: /etc: Is a directory"
+  assert_line --index 1 "bash: line 1: exec: /etc: cannot execute: Is a directory"
+  assert_line --index 2 "Error: failed to invoke command /etc in container $(get_latest_container_name)"
+  assert [ ${#stderr_lines[@]} -eq 3 ]
 }
 
-@test "run: Try to run non-existent command in the default container" {
+@test "run: Try a non-existent command" {
   local cmd="non-existent-command"
 
   create_default_container
 
-  run -127 $TOOLBOX run $cmd
+  run -127 --separate-stderr $TOOLBOX run $cmd
 
   assert_failure
-  assert [ $status -eq 127 ]
-  assert_line --index 0 "/bin/sh: line 1: exec: $cmd: not found"
+  assert [ ${#lines[@]} -eq 0 ]
+  lines=("${stderr_lines[@]}")
+  assert_line --index 0 "bash: line 1: exec: $cmd: not found"
   assert_line --index 1 "Error: command $cmd not found in container $(get_latest_container_name)"
-  assert [ ${#lines[@]} -eq 2 ]
-}
-
-@test "run: Try to run /etc as a command in the deault container" {
-  create_default_container
-
-  run $TOOLBOX run /etc
-
-  assert_failure
-  assert [ $status -eq 126 ]
-  assert_line --index 0 "/bin/sh: line 1: /etc: Is a directory"
-  assert_line --index 1 "/bin/sh: line 1: exec: /etc: cannot execute: Is a directory"
-  assert_line --index 2 "Error: failed to invoke command /etc in container $(get_latest_container_name)"
-  assert [ ${#lines[@]} -eq 3 ]
+  assert [ ${#stderr_lines[@]} -eq 2 ]
 }