diff --git a/test/cases/api.sh b/test/cases/api.sh
index bbe1c3dea..7ea18b4f8 100755
--- a/test/cases/api.sh
+++ b/test/cases/api.sh
@@ -330,6 +330,43 @@ EndOfMessage
 fi
 export SUBSCRIPTION_BLOCK
 
+# Define the customizations for the images here to not have to repeat them
+# in every image-type specific file.
+case "${IMAGE_TYPE}" in
+  # The Directories and Files customization is not supported for this image type.
+  "$IMAGE_TYPE_EDGE_INSTALLER")
+    DIR_FILES_CUSTOMIZATION_BLOCK=
+    ;;
+  *)
+    DIR_FILES_CUSTOMIZATION_BLOCK=$(cat <<EOF
+,
+    "directories": [
+      {
+        "path": "/etc/custom_dir/dir1",
+        "user": "root",
+        "group": "root",
+        "mode": "0775",
+        "ensure_parents": true
+      },
+      {
+        "path": "/etc/custom_dir2"
+      }
+    ],
+    "files": [
+      {
+        "path": "/etc/custom_dir/custom_file.txt",
+        "data": "image builder is the best\n"
+      },
+      {
+        "path": "/etc/custom_dir2/empty_file.txt"
+      }
+    ]
+EOF
+)
+    ;;
+esac
+export DIR_FILES_CUSTOMIZATION_BLOCK
+
 # generate a temp key for user tests
 ssh-keygen -t rsa-sha2-512 -f "${WORKDIR}/usertest" -C "usertest" -N ""
 
diff --git a/test/cases/api/aws.sh b/test/cases/api/aws.sh
index 981a1342b..4a44dbd08 100644
--- a/test/cases/api/aws.sh
+++ b/test/cases/api/aws.sh
@@ -52,7 +52,7 @@ function createReqFile() {
     "packages": [
       "postgresql",
       "dummy"
-    ]${SUBSCRIPTION_BLOCK},
+    ],
     "users":[
       {
         "name": "user1",
@@ -63,7 +63,7 @@ function createReqFile() {
         "name": "user2",
         "key": "$(cat "${WORKDIR}/usertest.pub")"
       }
-    ]
+    ]${SUBSCRIPTION_BLOCK}${DIR_FILES_CUSTOMIZATION_BLOCK}
   },
   "image_request": {
       "architecture": "$ARCH",
diff --git a/test/cases/api/azure.sh b/test/cases/api/azure.sh
index 329756b91..d15592d40 100644
--- a/test/cases/api/azure.sh
+++ b/test/cases/api/azure.sh
@@ -84,7 +84,7 @@ function createReqFile() {
     "packages": [
       "postgresql",
       "dummy"
-    ]${SUBSCRIPTION_BLOCK}
+    ]${SUBSCRIPTION_BLOCK}${DIR_FILES_CUSTOMIZATION_BLOCK}
   },
   "image_request": {
     "architecture": "$ARCH",
diff --git a/test/cases/api/common/common.sh b/test/cases/api/common/common.sh
index 0051b83e5..7bfa4e948 100644
--- a/test/cases/api/common/common.sh
+++ b/test/cases/api/common/common.sh
@@ -43,6 +43,9 @@ function _instanceCheck() {
   else
     echo "Not RHEL OS. Skip subscription check."
   fi
+
+  # Verify that directories and files customization worked as expected
+  verify_dirs_files_customization "$_ssh"
 }
 
 WORKER_REFRESH_TOKEN_PATH="/etc/osbuild-worker/token"
@@ -90,3 +93,39 @@ function compose_status_with_org_id {
     --header "Authorization: Bearer $(access_token_with_org_id "$refresh_token")" \
     "http://localhost:443/api/image-builder-composer/v2/composes/$compose"
 }
+
+# Verify that directories and files customization worked as expected
+function verify_dirs_files_customization {
+  echo "✔️ Checking custom directories and files"
+  local _ssh="$1"
+  local _error=0
+
+  # verify that `/etc/custom_dir/dir1` exists and has mode `0775`
+  local cust_dir1_mode
+  cust_dir1_mode=$($_ssh stat -c '%a' /etc/custom_dir/dir1)
+  if [[ "$cust_dir1_mode" != "775" ]]; then
+    echo "Directory /etc/custom_dir/dir1 has wrong mode: $cust_dir1_mode"
+    _error=1
+  fi
+
+  # verify that `/etc/custom_dir/custom_file.txt` exists and contains `image builder is the best\n`
+  local cust_file_content
+  cust_file_content=$($_ssh cat /etc/custom_dir/custom_file.txt)
+  if [[ "$cust_file_content" != "image builder is the best" ]]; then
+    echo "File /etc/custom_dir/custom_file.txt has wrong content: $cust_file_content"
+    _error=1
+  fi
+
+  # verify that `/etc/custom_dir2/empty_file.txt` exists and is empty
+  local cust_file2_content
+  cust_file2_content=$($_ssh cat /etc/custom_dir2/empty_file.txt)
+  if [[ "$cust_file2_content" != "" ]]; then
+    echo "File /etc/custom_dir2/empty_file.txt has wrong content: $cust_file2_content"
+    _error=1
+  fi
+
+  if [[ "$_error" == "1" ]]; then
+    echo "Testing of custom directories and files failed."
+    exit 1
+  fi
+}
diff --git a/test/cases/api/common/s3.sh b/test/cases/api/common/s3.sh
index 0a924369f..f943da40d 100644
--- a/test/cases/api/common/s3.sh
+++ b/test/cases/api/common/s3.sh
@@ -37,7 +37,7 @@ function createReqFileEdge() {
         "name": "user2",
         "key": "$(cat "${WORKDIR}/usertest.pub")"
       }
-    ]
+    ]${DIR_FILES_CUSTOMIZATION_BLOCK}
   },
   "image_request": {
     "architecture": "$ARCH",
@@ -67,7 +67,7 @@ function createReqFileGuest() {
     "packages": [
       "postgresql",
       "dummy"
-    ]${SUBSCRIPTION_BLOCK},
+    ],
     "users":[
       {
         "name": "user1",
@@ -78,7 +78,7 @@ function createReqFileGuest() {
         "name": "user2",
         "key": "$(cat "${WORKDIR}/usertest.pub")"
       }
-    ]
+    ]${SUBSCRIPTION_BLOCK}${DIR_FILES_CUSTOMIZATION_BLOCK}
   },
   "image_request": {
     "architecture": "$ARCH",
@@ -107,7 +107,7 @@ function createReqFileVSphere() {
     "packages": [
       "postgresql",
       "dummy"
-    ]${SUBSCRIPTION_BLOCK}
+    ]${SUBSCRIPTION_BLOCK}${DIR_FILES_CUSTOMIZATION_BLOCK}
   },
   "image_request": {
     "architecture": "$ARCH",
@@ -156,6 +156,44 @@ function verifyEdgeCommit() {
         exit 1
     fi
 
+    verify_dirs_files_customization_edge_commit "${COMMIT_DIR}/repo" $OSTREE_REF
+}
+
+function verify_dirs_files_customization_edge_commit() {
+  echo "✔️ Checking custom directories and files is ostree commit"
+  local _repo_path=$1
+  local _ref=$2
+  local _error=0
+
+  # verify that `/usr/etc/custom_dir/dir1` exists and has mode `0775`
+  # the output from ostree is 'd00775 0 0      0 { [(b'security.selinux', b'system_u:object_r:etc_t:s0')] } /usr/etc/custom_dir/dir1'
+  local cust_dir1_mode
+  cust_dir1_mode=$(ostree --repo="${_repo_path}" ls -X "${_ref}" /usr/etc/custom_dir/dir1 | awk '{print $1}')
+  if [[ "$cust_dir1_mode" != "d00775" ]]; then
+    echo "Directory /usr/etc/custom_dir/dir1 has wrong mode: $cust_dir1_mode"
+    _error=1
+  fi
+
+  # verify that `/usr/etc/custom_dir/custom_file.txt` exists and contains `image builder is the best\n`
+  local cust_file_content
+  cust_file_content=$(ostree --repo="${_repo_path}" cat "${_ref}" /usr/etc/custom_dir/custom_file.txt)
+  if [[ "$cust_file_content" != "image builder is the best" ]]; then
+    echo "File /usr/etc/custom_dir/custom_file.txt has wrong content: $cust_file_content"
+    _error=1
+  fi
+
+  # verify that `/usr/etc/custom_dir2/empty_file.txt` exists and is empty
+  local cust_file2_content
+  cust_file2_content=$(ostree --repo="${_repo_path}" cat "${_ref}" /usr/etc/custom_dir2/empty_file.txt)
+  if [[ "$cust_file2_content" != "" ]]; then
+    echo "File /usr/etc/custom_dir2/empty_file.txt has wrong content: $cust_file2_content"
+    _error=1
+  fi
+
+  if [[ "$_error" == "1" ]]; then
+    echo "Testing of custom directories and files failed."
+    exit 1
+  fi
 }
 
 # Verify image blobs from s3
diff --git a/test/cases/api/gcp.sh b/test/cases/api/gcp.sh
index 90221c481..a0e0235ca 100644
--- a/test/cases/api/gcp.sh
+++ b/test/cases/api/gcp.sh
@@ -71,7 +71,7 @@ function createReqFile() {
     "packages": [
       "postgresql",
       "dummy"
-    ]${SUBSCRIPTION_BLOCK}
+    ]${SUBSCRIPTION_BLOCK}${DIR_FILES_CUSTOMIZATION_BLOCK}
   },
   "image_request": {
     "architecture": "$ARCH",