diff --git a/.bazelci/presubmit.yml b/.bazelci/presubmit.yml
index 0d1da3ee2e..a08e71c25e 100644
--- a/.bazelci/presubmit.yml
+++ b/.bazelci/presubmit.yml
@@ -13,6 +13,9 @@ nightly_aspects_flags: &nightly_aspects_flags
   - "--config=clippy"
 bzlmod_flags: &bzlmod_flags
   - "--lockfile_mode=error"
+bzlmod_plus_repo_names_flags: &bzlmod_plus_repo_names_flags
+  # `--lockfile_mode=error` is omitted because the repo names leak into the lock file.
+  - "--incompatible_use_plus_in_repo_names"
 single_rust_channel_targets: &single_rust_channel_targets
   - "--"
   - "//..."
@@ -753,6 +756,46 @@ tasks:
       - "@rules_rust//tools/rust_analyzer:gen_rust_project"
     test_targets:
       - "//..."
+  ubuntu2004_bzlmod_plus_repo_names_bcr:
+    name: bzlmod BCR presubmit w/ incompatible flags
+    # A newer version than is specified in the .bazel_version file is needed for
+    # --incompatible_use_plus_in_repo_names'
+    bazel: *minimum_bazel_version
+    platform: ubuntu2004
+    working_directory: examples/bzlmod/hello_world
+    test_flags: *bzlmod_plus_repo_names_flags
+    run_targets:
+      - "//third-party:vendor"
+      - "@rules_rust//tools/rust_analyzer:gen_rust_project"
+    test_targets:
+      - "//..."
+  macos_bzlmod_plus_repo_names_bcr:
+    name: bzlmod BCR presubmit w/ incompatible flags
+    # A newer version than is specified in the .bazel_version file is needed for
+    # --incompatible_use_plus_in_repo_names'
+    bazel: *minimum_bazel_version
+    platform: macos
+    working_directory: examples/bzlmod/hello_world
+    test_flags: *bzlmod_plus_repo_names_flags
+    run_targets:
+      - "//third-party:vendor"
+      - "@rules_rust//tools/rust_analyzer:gen_rust_project"
+    test_targets:
+      - "//..."
+  windows_bzlmod_plus_repo_names_bcr:
+    name: bzlmod BCR presubmit w/ incompatible flags
+    # A newer version than is specified in the .bazel_version file is needed for
+    # --incompatible_use_plus_in_repo_names'
+    bazel: *minimum_bazel_version
+    platform: windows
+    working_directory: examples/bzlmod/hello_world
+    test_flags: *bzlmod_plus_repo_names_flags
+    run_targets:
+      - "//third-party:vendor"
+    build_targets:
+      - "@rules_rust//tools/rust_analyzer:gen_rust_project"
+    test_targets:
+      - "//..."
   bzlmod_no_cargo:
     name: Cargo-less bzlmod
     platform: ubuntu2004
diff --git a/crate_universe/src/utils.rs b/crate_universe/src/utils.rs
index d625e0572c..041b8f5655 100644
--- a/crate_universe/src/utils.rs
+++ b/crate_universe/src/utils.rs
@@ -34,7 +34,6 @@ pub(crate) fn normalize_cargo_file_paths(
     outputs
         .into_iter()
         .map(|(path, content)| {
-            let path = out_dir.join(path);
             // Get Path Str and Parent Path Str so we can rename the root file
             let original_path_str = path.to_str().expect("All file paths should be strings");
             let original_parent_path_str = path
@@ -43,16 +42,23 @@ pub(crate) fn normalize_cargo_file_paths(
                 .to_str()
                 .expect("All file paths should be strings");
 
-            let new_path = if original_parent_path_str.contains('+') {
+            let path = if original_parent_path_str.contains('+') {
                 let new_parent_file_path = sanitize_repository_name(original_parent_path_str);
-                std::fs::rename(original_parent_path_str, new_parent_file_path)
-                    .expect("Could not rename paths");
+                std::fs::rename(
+                    out_dir.join(original_parent_path_str),
+                    out_dir.join(new_parent_file_path),
+                )
+                .expect("Could not rename paths");
                 PathBuf::from(&original_path_str.replace('+', "-"))
             } else {
                 path
             };
 
-            (new_path, content)
+            // In recent versions of Bazel, canonical repository paths may contain (+)
+            // symbols so it is important to apply the transformation only to `outputs`
+            // and leave `out_dir` untouched.
+            let path = out_dir.join(path);
+            (path, content)
         })
         .collect()
 }