diff --git a/misc/diff-cache.py b/misc/diff-cache.py
index 7e33e17fd909..1f1b2a39c4bb 100644
--- a/misc/diff-cache.py
+++ b/misc/diff-cache.py
@@ -115,7 +115,7 @@ def load(cache: MetadataStore, s: str) -> Any:
             return data
         normalize_meta(meta)
         return serialize_meta_ff(meta, version_prefix)
-    if s.endswith(".data.ff"):
+    if s.endswith((".data.ff", ".err.ff")):
         return data
     obj = json_loads(data)
     if s.endswith(".meta.json"):
diff --git a/mypy/build.py b/mypy/build.py
index 4fe6f52f5828..f079d3a63663 100644
--- a/mypy/build.py
+++ b/mypy/build.py
@@ -69,6 +69,7 @@
     Tag,
     WriteBuffer,
     read_bytes,
+    read_errors,
     read_int,
     read_int_list,
     read_int_opt,
@@ -76,6 +77,7 @@
     read_str_list,
     read_str_opt,
     write_bytes,
+    write_errors,
     write_int,
     write_int_list,
     write_int_opt,
@@ -1626,6 +1628,13 @@ def create_metastore(options: Options, parallel_worker: bool = False) -> Metadat
     return mds
 
 
+def get_errors_name(meta_name: str) -> str:
+    # Convert e.g. foo.bar.meta.ff to foo.bar.err.ff
+    parts = meta_name.rsplit(".", maxsplit=2)
+    parts[1] = "err"
+    return ".".join(parts)
+
+
 def get_cache_names(id: str, path: str, options: Options) -> tuple[str, str, str | None]:
     """Return the file names for the cache files.
 
@@ -1688,7 +1697,7 @@ def options_snapshot(id: str, manager: BuildManager) -> dict[str, object]:
 
 def find_cache_meta(
     id: str, path: str, manager: BuildManager, skip_validation: bool = False
-) -> CacheMeta | None:
+) -> tuple[CacheMeta | None, list[ErrorTuple]]:
     """Find cache data for a module.
 
     Args:
@@ -1705,15 +1714,12 @@ def find_cache_meta(
     meta_file, data_file, _ = get_cache_names(id, path, manager.options)
     if manager.tracing_enabled:
         manager.trace(f"Looking for {id} at {meta_file}")
-    meta: bytes | dict[str, Any] | None
     if manager.stats_enabled:
         t0 = time.time()
     if manager.options.fixed_format_cache:
         meta = _load_ff_file(
             meta_file, manager, log_error_fmt="Could not load cache for {}: ", id=id
         )
-        if meta is None:
-            return None
     else:
         meta = _load_json_file(
             meta_file,
@@ -1721,13 +1727,8 @@ def find_cache_meta(
             log_success=f"Meta {id} ",
             log_error=f"Could not load cache for {id}: ",
         )
-        if meta is None:
-            return None
-        if not isinstance(meta, dict):
-            manager.log(  # type: ignore[unreachable]
-                f"Could not load cache for {id}: meta cache is not a dict: {repr(meta)}"
-            )
-            return None
+    if meta is None:
+        return None, []
     if manager.stats_enabled:
         t1 = time.time()
     if isinstance(meta, bytes):
@@ -1736,31 +1737,31 @@ def find_cache_meta(
         # TODO: switch to something like librt.internal.read_byte() if this is slow.
         if meta[0] != cache_version() or meta[1] != CACHE_VERSION:
             manager.log(f"Metadata abandoned for {id}: incompatible cache format")
-            return None
+            return None, []
         data_io = ReadBuffer(meta[2:])
         m = CacheMeta.read(data_io, data_file)
     else:
         m = CacheMeta.deserialize(meta, data_file)
     if m is None:
         manager.log(f"Metadata abandoned for {id}: cannot deserialize data")
-        return None
+        return None, []
     if manager.stats_enabled:
         t2 = time.time()
         manager.add_stats(
             load_meta_time=t2 - t0, load_meta_load_time=t1 - t0, load_meta_from_dict_time=t2 - t1
         )
     if skip_validation:
-        return m
+        return m, []
 
     # Ignore cache if generated by an older mypy version.
     if m.version_id != manager.version_id and not manager.options.skip_version_check:
         manager.log(f"Metadata abandoned for {id}: different mypy version")
-        return None
+        return None, []
 
     total_deps = len(m.dependencies) + len(m.suppressed)
     if len(m.dep_prios) != total_deps or len(m.dep_lines) != total_deps:
         manager.log(f"Metadata abandoned for {id}: broken dependencies")
-        return None
+        return None, []
 
     # Ignore cache if (relevant) options aren't the same.
     # Note that it's fine to mutilate cached_options since it's only used here.
@@ -1782,12 +1783,12 @@ def find_cache_meta(
                             key, cached_options.get(key), current_options.get(key)
                         )
                     )
-        return None
+        return None, []
     if manager.old_plugins_snapshot and manager.plugins_snapshot:
         # Check if plugins are still the same.
         if manager.plugins_snapshot != manager.old_plugins_snapshot:
             manager.log(f"Metadata abandoned for {id}: plugins differ")
-            return None
+            return None, []
     plugin_data = manager.plugin.report_config_data(ReportConfigContext(id, path, is_check=True))
     if not manager.options.fixed_format_cache:
         # So that plugins can return data with tuples in it without
@@ -1796,10 +1797,31 @@ def find_cache_meta(
         plugin_data = json_loads(json_dumps(plugin_data))
     if m.plugin_data != plugin_data:
         manager.log(f"Metadata abandoned for {id}: plugin configuration differs")
-        return None
+        return None, []
 
+    # Load cached errors for this file, even if empty. This is needed to avoid
+    # invalid cache state after a crash/blocker/Ctrl+C etc.
+    errors_file = get_errors_name(meta_file)
+    if manager.options.fixed_format_cache:
+        errors = _load_ff_file(
+            errors_file, manager, log_error_fmt="Could not load errors for {}: ", id=id
+        )
+    else:
+        errors = _load_json_file(
+            errors_file,
+            manager,
+            log_success=f"Errors {id} ",
+            log_error=f"Could not load errors for {id}: ",
+        )
+    if errors is None:
+        return None, []
+    if isinstance(errors, bytes):
+        data_io = ReadBuffer(errors)
+        e = read_errors(data_io)
+    else:
+        e = [tuple(err) for err in errors["error_lines"]]
     manager.add_stats(fresh_metas=1)
-    return m
+    return m, e
 
 
 def validate_meta(
@@ -2078,9 +2100,8 @@ def write_cache(
         version_id=manager.version_id,
         ignore_all=ignore_all,
         plugin_data=plugin_data,
-        # These two will be filled by the caller.
+        # This one will be filled by the caller.
         dep_hashes=[],
-        error_lines=[],
     )
     return interface_hash, (meta, meta_file)
 
@@ -2104,6 +2125,23 @@ def write_cache_meta(meta: CacheMeta, manager: BuildManager, meta_file: str) ->
         manager.log(f"Error writing cache meta file {meta_file}")
 
 
+def write_errors_file(
+    meta_file: str, error_lines: list[ErrorTuple], manager: BuildManager
+) -> None:
+    # Write errors cache file
+    errors_file = get_errors_name(meta_file)
+    metastore = manager.metastore
+    if manager.options.fixed_format_cache:
+        data_io = WriteBuffer()
+        write_errors(data_io, error_lines)
+        meta_bytes = data_io.getvalue()
+    else:
+        # Some generic JSON helpers require top-level to be a dict.
+        meta_bytes = json_dumps({"error_lines": error_lines}, manager.options.debug_cache)
+    if not metastore.write(errors_file, meta_bytes):
+        manager.log(f"Error writing errors file {errors_file}")
+
+
 """Dependency manager.
 
 Design
@@ -2393,7 +2431,7 @@ def new_state(
         interface_hash = b""
         meta_source_hash = None
         if path and source is None and manager.cache_enabled:
-            meta = find_cache_meta(id, path, manager)
+            meta, error_lines = find_cache_meta(id, path, manager)
             # TODO: Get mtime if not cached.
             if meta is not None:
                 interface_hash = meta.interface_hash
@@ -2420,7 +2458,7 @@ def new_state(
             assert len(meta.dep_hashes) == len(meta.dependencies)
             dep_hashes = {k: v for (k, v) in zip(meta.dependencies, meta.dep_hashes)}
             # Only copy `error_lines` if the module is not silently imported.
-            error_lines = [] if ignore_all else meta.error_lines
+            error_lines = [] if ignore_all else error_lines
             imports_ignored = meta.imports_ignored
         else:
             dependencies = []
@@ -2656,7 +2694,7 @@ def reload_meta(self) -> None:
         the interface hash.
         """
         assert self.path is not None
-        self.meta = find_cache_meta(self.id, self.path, self.manager, skip_validation=True)
+        self.meta, _ = find_cache_meta(self.id, self.path, self.manager, skip_validation=True)
         assert self.meta is not None
         self.interface_hash = self.meta.interface_hash
 
@@ -4355,8 +4393,8 @@ def process_stale_scc(
             continue
         meta, meta_file = meta_tuple
         meta.dep_hashes = [graph[dep].interface_hash for dep in graph[id].dependencies]
-        meta.error_lines = errors_by_id.get(id, [])
         write_cache_meta(meta, manager, meta_file)
+        write_errors_file(meta_file, errors_by_id.get(id, []), manager)
     manager.done_sccs.add(ascc.id)
     manager.add_stats(
         load_missing_time=t1 - t0,
diff --git a/mypy/cache.py b/mypy/cache.py
index 5a1d6c79219e..0adc7affb8cb 100644
--- a/mypy/cache.py
+++ b/mypy/cache.py
@@ -69,7 +69,7 @@
 from mypy_extensions import u8
 
 # High-level cache layout format
-CACHE_VERSION: Final = 6
+CACHE_VERSION: Final = 7
 
 # Type used internally to represent errors:
 #   (path, line, column, end_line, end_column, severity, message, code)
@@ -99,7 +99,6 @@ def __init__(
         dep_hashes: list[bytes],
         interface_hash: bytes,
         trans_dep_hash: bytes,
-        error_lines: list[ErrorTuple],
         version_id: str,
         ignore_all: bool,
         plugin_data: Any,
@@ -123,7 +122,6 @@ def __init__(
         self.dep_hashes = dep_hashes  # list of interface_hash for dependencies
         self.interface_hash = interface_hash  # hash representing the public interface
         self.trans_dep_hash = trans_dep_hash  # hash of import structure (transitive)
-        self.error_lines = error_lines
         self.version_id = version_id  # mypy version for cache invalidation
         self.ignore_all = ignore_all  # if errors were ignored
         self.plugin_data = plugin_data  # config data from plugins
@@ -146,7 +144,6 @@ def serialize(self) -> dict[str, Any]:
             "dep_hashes": [dep.hex() for dep in self.dep_hashes],
             "interface_hash": self.interface_hash.hex(),
             "trans_dep_hash": self.trans_dep_hash.hex(),
-            "error_lines": self.error_lines,
             "version_id": self.version_id,
             "ignore_all": self.ignore_all,
             "plugin_data": self.plugin_data,
@@ -175,7 +172,6 @@ def deserialize(cls, meta: dict[str, Any], data_file: str) -> CacheMeta | None:
                 dep_hashes=[bytes.fromhex(dep) for dep in meta["dep_hashes"]],
                 interface_hash=bytes.fromhex(meta["interface_hash"]),
                 trans_dep_hash=bytes.fromhex(meta["trans_dep_hash"]),
-                error_lines=[tuple(err) for err in meta["error_lines"]],
                 version_id=meta["version_id"],
                 ignore_all=meta["ignore_all"],
                 plugin_data=meta["plugin_data"],
@@ -203,7 +199,6 @@ def write(self, data: WriteBuffer) -> None:
         write_bytes_list(data, self.dep_hashes)
         write_bytes(data, self.interface_hash)
         write_bytes(data, self.trans_dep_hash)
-        write_errors(data, self.error_lines)
         write_str(data, self.version_id)
         write_bool(data, self.ignore_all)
         # Plugin data may be not a dictionary, so we use
@@ -233,7 +228,6 @@ def read(cls, data: ReadBuffer, data_file: str) -> CacheMeta | None:
                 dep_hashes=read_bytes_list(data),
                 interface_hash=read_bytes(data),
                 trans_dep_hash=read_bytes(data),
-                error_lines=read_errors(data),
                 version_id=read_str(data),
                 ignore_all=read_bool(data),
                 plugin_data=read_json_value(data),
diff --git a/mypy/exportjson.py b/mypy/exportjson.py
index 922b3ecb3088..c08f0f9f2911 100644
--- a/mypy/exportjson.py
+++ b/mypy/exportjson.py
@@ -572,7 +572,6 @@ def convert_binary_cache_meta_to_json(data: bytes, data_file: str) -> Json:
         "dep_lines": meta.dep_lines,
         "dep_hashes": [dep.hex() for dep in meta.dep_hashes],
         "interface_hash": meta.interface_hash.hex(),
-        "error_lines": meta.error_lines,
         "version_id": meta.version_id,
         "ignore_all": meta.ignore_all,
         "plugin_data": meta.plugin_data,
diff --git a/mypy/test/test_diff_cache.py b/mypy/test/test_diff_cache.py
index a62c3a18c696..d35cd99f342d 100644
--- a/mypy/test/test_diff_cache.py
+++ b/mypy/test/test_diff_cache.py
@@ -127,7 +127,7 @@ def test_diff_cache_produces_valid_json(self) -> None:
             a_keys = {k for k in keys if "/a." in k or k.startswith("a.")}
             assert len(a_keys) == 0, f"Unexpected a.* entries in diff: {a_keys}"
             assert len(b_keys) == 2, f"Expected 2 b.* entries in diff, got: {b_keys}"
-            assert len(c_keys) == 3, f"Expected 3 c.* entries in diff, got: {c_keys}"
+            assert len(c_keys) == 4, f"Expected 3 c.* entries in diff, got: {c_keys}"
 
             # The new access to a.x in b.py should create a fine-grained
             # dependency recorded in @root.deps.json.
diff --git a/mypy/test/testcheck.py b/mypy/test/testcheck.py
index cbb9c0235fed..96d6f536b961 100644
--- a/mypy/test/testcheck.py
+++ b/mypy/test/testcheck.py
@@ -293,7 +293,7 @@ def find_missing_cache_files(
         ignore_errors = True
         missing = {}
         for id, path in modules.items():
-            meta = build.find_cache_meta(id, path, manager)
+            meta, _ = build.find_cache_meta(id, path, manager)
             if not build.validate_meta(meta, id, path, ignore_errors, manager):
                 missing[id] = path
         return set(missing.values())
diff --git a/test-data/unit/exportjson.test b/test-data/unit/exportjson.test
index 43e061dfda32..2d6a8c56b20f 100644
--- a/test-data/unit/exportjson.test
+++ b/test-data/unit/exportjson.test
@@ -317,7 +317,6 @@ from typing_extensions import Final
         "<hash>"
     ],
     "interface_hash": "<hash>",
-    "error_lines": [],
     "version_id": ...,
     "ignore_all": false,
     "plugin_data": null