diff --git a/_pytest/config.py b/_pytest/config.py
index d97771155a..359cc4bc84 100644
--- a/_pytest/config.py
+++ b/_pytest/config.py
@@ -1327,10 +1327,14 @@ def determine_setup(inifile, args, warnfunc=None):
     dirs = get_dirs_from_args(args)
     if inifile:
         iniconfig = py.iniconfig.IniConfig(inifile)
-        try:
-            inicfg = iniconfig["pytest"]
-        except KeyError:
-            inicfg = None
+        is_cfg_file = str(inifile).endswith('.cfg')
+        sections = ['tool:pytest', 'pytest'] if is_cfg_file else ['pytest']
+        for section in sections:
+            try:
+                inicfg = iniconfig[section]
+                break
+            except KeyError:
+                inicfg = None
         rootdir = get_common_ancestor(dirs)
     else:
         ancestor = get_common_ancestor(dirs)
diff --git a/changelog/3260.bugfix.rst b/changelog/3260.bugfix.rst
new file mode 100644
index 0000000000..eb0ecd3457
--- /dev/null
+++ b/changelog/3260.bugfix.rst
@@ -0,0 +1 @@
+``[tool:pytest]`` sections in ``*.cfg`` files passed by the ``-c`` option are now properly recognized.
diff --git a/testing/test_config.py b/testing/test_config.py
index f256b512f5..39105f5d68 100644
--- a/testing/test_config.py
+++ b/testing/test_config.py
@@ -110,6 +110,13 @@ def pytest_addoption(parser):
         config = testdir.parseconfig("-c", "custom.cfg")
         assert config.getini("custom") == "1"
 
+        testdir.makefile(".cfg", custom_tool_pytest_section="""
+            [tool:pytest]
+            custom = 1
+        """)
+        config = testdir.parseconfig("-c", "custom_tool_pytest_section.cfg")
+        assert config.getini("custom") == "1"
+
     def test_absolute_win32_path(self, testdir):
         temp_cfg_file = testdir.makefile(".cfg", custom="""
             [pytest]