diff --git a/mypy/dmypy_server.py b/mypy/dmypy_server.py
index da0edff7240c..2a62483e0b89 100644
--- a/mypy/dmypy_server.py
+++ b/mypy/dmypy_server.py
@@ -253,8 +253,7 @@ def check_fine_grained(self, sources: List[mypy.build.BuildSource]) -> Dict[str,
     def initialize_fine_grained(self, sources: List[mypy.build.BuildSource]) -> Dict[str, Any]:
         # The file system cache we create gets passed off to
         # BuildManager, and thence to FineGrainedBuildManager, which
-        # assumes responsibility for clearing it at the appropriate
-        # times (after init and update()).
+        # assumes responsibility for clearing it after updates.
         fscache = FileSystemCache(self.options.python_version)
         self.fswatcher = FileSystemWatcher(fscache)
         self.update_sources(sources)
@@ -295,6 +294,7 @@ def initialize_fine_grained(self, sources: List[mypy.build.BuildSource]) -> Dict
             # Run an update
             messages = self.fine_grained_manager.update(self.find_changed(sources))
 
+        fscache.flush()
         status = 1 if messages else 0
         return {'out': ''.join(s + '\n' for s in messages), 'err': '', 'status': status}
 
diff --git a/mypy/server/update.py b/mypy/server/update.py
index 6c80cb9ee838..4bf625ed3774 100644
--- a/mypy/server/update.py
+++ b/mypy/server/update.py
@@ -175,7 +175,6 @@ def __init__(self, result: BuildResult) -> None:
         manager.saved_cache = {}
         # Active triggers during the last update
         self.triggered = []  # type: List[str]
-        self.manager.fscache.flush()
 
     def update(self, changed_modules: List[Tuple[str, str]]) -> List[str]:
         """Update previous build result by processing changed modules.
diff --git a/mypy/test/testfinegrained.py b/mypy/test/testfinegrained.py
index 83512cf0837f..7ffc3bef159c 100644
--- a/mypy/test/testfinegrained.py
+++ b/mypy/test/testfinegrained.py
@@ -86,6 +86,7 @@ def run_case(self, testcase: DataDrivenTestCase) -> None:
 
         fine_grained_manager = None
         if not self.use_cache:
+            result.manager.fscache.flush()
             fine_grained_manager = FineGrainedBuildManager(result)
             if CHECK_CONSISTENCY:
                 check_consistency(fine_grained_manager)
diff --git a/mypy/test/testmerge.py b/mypy/test/testmerge.py
index 50d9d97a8a76..18fc51d8cbb3 100644
--- a/mypy/test/testmerge.py
+++ b/mypy/test/testmerge.py
@@ -69,6 +69,7 @@ def run_case(self, testcase: DataDrivenTestCase) -> None:
         main_src = '\n'.join(testcase.input)
         result = self.build(main_src)
         assert result is not None, 'cases where CompileError occurred should not be run'
+        result.manager.fscache.flush()
         fine_grained_manager = FineGrainedBuildManager(result)
 
         a = []