diff --git a/atst/app.py b/atst/app.py
index 1b60f64c..e9daabd6 100644
--- a/atst/app.py
+++ b/atst/app.py
@@ -200,23 +200,21 @@ def make_config(direct_config=None):
     ENV_CONFIG_FILENAME = os.path.join(
         os.path.dirname(__file__), "../config/", "{}.ini".format(ENV.lower())
     )
-    OVERRIDE_CONFIG_FILENAME = os.getenv("OVERRIDE_CONFIG_FULLPATH")
+    OVERRIDE_CONFIG_DIRECTORY = os.getenv("OVERRIDE_CONFIG_DIRECTORY")
 
     config = ConfigParser(allow_no_value=True)
     config.optionxform = str
 
     config_files = [BASE_CONFIG_FILENAME, ENV_CONFIG_FILENAME]
-    if OVERRIDE_CONFIG_FILENAME:
-        config_files.append(OVERRIDE_CONFIG_FILENAME)
 
     # ENV_CONFIG will override values in BASE_CONFIG.
     config.read(config_files)
 
+    if OVERRIDE_CONFIG_DIRECTORY:
+        apply_config_from_directory(OVERRIDE_CONFIG_DIRECTORY, config)
+
     # Check for ENV variables as a final source of overrides
-    for confsetting in config.options("default"):
-        env_override = os.getenv(confsetting.upper())
-        if env_override:
-            config.set("default", confsetting, env_override)
+    apply_config_from_environment(config)
 
     # override if a dictionary of options has been given
     if direct_config:
@@ -244,6 +242,36 @@ def make_config(direct_config=None):
     return map_config(config)
 
 
+def apply_config_from_directory(config_dir, config, section="default"):
+    """
+    Loop files in a directory, check if the names correspond to
+    known config values, and apply the file contents as the value
+    for that setting if they do.
+    """
+    for confsetting in os.listdir(config_dir):
+        if confsetting in config.options(section):
+            full_path = os.path.join(config_dir, confsetting)
+            with open(full_path, "r") as conf_file:
+                config.set(section, confsetting, conf_file.read().strip())
+
+    return config
+
+
+def apply_config_from_environment(config, section="default"):
+    """
+    Loops all the configuration settins in a given section of a
+    config object and checks whether those settings also exist as
+    environment variables. If so, it applies the environment
+    variables value as the new configuration setting value.
+    """
+    for confsetting in config.options(section):
+        env_override = os.getenv(confsetting.upper())
+        if env_override:
+            config.set(section, confsetting, env_override)
+
+    return config
+
+
 def make_redis(app, config):
     r = redis.Redis.from_url(config["REDIS_URI"])
     app.redis = r
diff --git a/tests/test_app.py b/tests/test_app.py
index 222f4a4f..937a15e2 100644
--- a/tests/test_app.py
+++ b/tests/test_app.py
@@ -1,8 +1,13 @@
 import os
 
+from configparser import ConfigParser
 import pytest
 
-from atst.app import make_crl_validator
+from atst.app import (
+    make_crl_validator,
+    apply_config_from_directory,
+    apply_config_from_environment,
+)
 
 
 @pytest.fixture
@@ -22,3 +27,43 @@ def test_make_crl_validator_creates_crl_dir(app, tmpdir, replace_crl_dir_config)
     replace_crl_dir_config(crl_dir)
     make_crl_validator(app)
     assert os.path.isdir(crl_dir)
+
+
+@pytest.fixture
+def config_object():
+    config = ConfigParser()
+    config.optionxform = str
+    config.read_string("[default]\nFOO=BALONEY")
+    return config
+
+
+def test_apply_config_from_directory(tmpdir, config_object):
+    config_setting = tmpdir.join("FOO")
+    with open(config_setting, "w") as conf_file:
+        conf_file.write("MAYO")
+
+    apply_config_from_directory(tmpdir, config_object)
+    assert config_object.get("default", "FOO") == "MAYO"
+
+
+def test_apply_config_from_directory_skips_unknown_settings(tmpdir, config_object):
+    config_setting = tmpdir.join("FLARF")
+    with open(config_setting, "w") as conf_file:
+        conf_file.write("MAYO")
+
+    apply_config_from_directory(tmpdir, config_object)
+    assert "FLARF" not in config_object.options("default")
+
+
+def test_apply_config_from_environment(monkeypatch, config_object):
+    monkeypatch.setenv("FOO", "MAYO")
+    apply_config_from_environment(config_object)
+    assert config_object.get("default", "FOO") == "MAYO"
+
+
+def test_apply_config_from_environment_skips_unknown_settings(
+    monkeypatch, config_object
+):
+    monkeypatch.setenv("FLARF", "MAYO")
+    apply_config_from_environment(config_object)
+    assert "FLARF" not in config_object.options("default")