diff --git a/apps/server/src/vcs/GitVcsDriverCore.test.ts b/apps/server/src/vcs/GitVcsDriverCore.test.ts
index 5cf3b7c4b4b9..9f4c344c7b8b 100644
--- a/apps/server/src/vcs/GitVcsDriverCore.test.ts
+++ b/apps/server/src/vcs/GitVcsDriverCore.test.ts
@@ -718,6 +718,67 @@ it.effect("refreshes the current branch after an external checkout", () =>
   ).pipe(Effect.provide(TestLayer)),
 );
 
+for (const configureWorktree of [false, true]) {
+  it.effect(
+    `keeps separate Git metadata out of worktree paths (core.worktree: ${configureWorktree})`,
+    () =>
+      Effect.scoped(
+        Effect.gen(function* () {
+          const driver = yield* GitVcsDriver.GitVcsDriver;
+          const fileSystem = yield* FileSystem.FileSystem;
+          const path = yield* Path.Path;
+          const cwd = yield* makeTmpDir();
+          const metadataRoot = yield* makeTmpDir("git-vcs-driver-metadata-");
+          const gitDir = path.join(metadataRoot, "metadata");
+          const { initialBranch } = yield* initRepoWithCommit(cwd);
+          yield* git(cwd, ["init", "--separate-git-dir", gitDir]);
+          if (configureWorktree) {
+            yield* git(cwd, ["config", "core.worktree", cwd]);
+          }
+          const nestedCwd = path.join(cwd, "nested");
+          yield* fileSystem.makeDirectory(nestedCwd);
+          const linkedPath = path.join(metadataRoot, "linked");
+          yield* git(cwd, ["worktree", "add", "-b", "linked", linkedPath]);
+
+          // Fill the shared ref cache from a linked checkout before reading the
+          // main checkout, whose root cannot be inferred from the metadata path.
+          const linkedRefs = yield* driver.listRefs({ cwd: linkedPath, refresh: true });
+          assert.equal(
+            linkedRefs.refs.find((ref) => ref.name === initialBranch)?.worktreePath,
+            null,
+          );
+          assert.equal(
+            NodeFS.realpathSync.native(
+              linkedRefs.refs.find((ref) => ref.name === "linked")!.worktreePath!,
+            ),
+            NodeFS.realpathSync.native(linkedPath),
+          );
+
+          const mainRefs = yield* driver.listRefs({ cwd: nestedCwd });
+          const mainRef = mainRefs.refs.find((ref) => ref.name === initialBranch);
+          assert.isTrue(mainRef?.current);
+          assert.equal(
+            NodeFS.realpathSync.native(mainRef!.worktreePath!),
+            NodeFS.realpathSync.native(cwd),
+          );
+          assert.equal(
+            NodeFS.realpathSync.native(
+              mainRefs.refs.find((ref) => ref.name === "linked")!.worktreePath!,
+            ),
+            NodeFS.realpathSync.native(linkedPath),
+          );
+
+          const linkedAgain = yield* driver.listRefs({ cwd: linkedPath });
+          assert.isTrue(linkedAgain.refs.find((ref) => ref.name === "linked")?.current);
+          assert.equal(
+            linkedAgain.refs.find((ref) => ref.name === initialBranch)?.worktreePath,
+            null,
+          );
+        }),
+      ).pipe(Effect.provide(TestLayer)),
+  );
+}
+
 it.effect("backs off failed upstream refreshes across linked worktrees", () =>
   Effect.scoped(
     Effect.gen(function* () {
diff --git a/apps/server/src/vcs/GitVcsDriverCore.ts b/apps/server/src/vcs/GitVcsDriverCore.ts
index 9367d027a210..392e7bcdd696 100644
--- a/apps/server/src/vcs/GitVcsDriverCore.ts
+++ b/apps/server/src/vcs/GitVcsDriverCore.ts
@@ -2772,10 +2772,14 @@ export const makeGitVcsDriverCore = Effect.fn("makeGitVcsDriverCore")(function*
     const existingWorktreeEntries = yield* Effect.filter(
       parsedWorktreeEntries,
       ([, worktreePath]) =>
-        fileSystem.stat(worktreePath).pipe(
-          Effect.as(true),
-          Effect.orElseSucceed(() => false),
-        ),
+        // With --separate-git-dir, Git can report the metadata directory as
+        // the main worktree. It must never be offered as a checkout to reuse.
+        worktreePath === gitCommonDir
+          ? Effect.succeed(false)
+          : fileSystem.stat(worktreePath).pipe(
+              Effect.as(true),
+              Effect.orElseSucceed(() => false),
+            ),
       { concurrency: 16 },
     );
     const worktreeMap = new Map(existingWorktreeEntries);
@@ -2964,12 +2968,18 @@ export const makeGitVcsDriverCore = Effect.fn("makeGitVcsDriverCore")(function*
       const hasCurrentWorktreeBranch =
         repositoryPaths.worktreeRoot !== null &&
         snapshot.localBranches.some((ref) => ref.worktreePath === repositoryPaths.worktreeRoot);
-      const localBranches = snapshot.localBranches.map((ref) => ({
-        ...ref,
-        current: hasCurrentWorktreeBranch
+      const localBranches = snapshot.localBranches.map((ref) => {
+        const current = hasCurrentWorktreeBranch
           ? ref.worktreePath === repositoryPaths.worktreeRoot
-          : ref.name === repositoryPaths.currentBranch,
-      }));
+          : ref.name === repositoryPaths.currentBranch;
+        return {
+          ...ref,
+          current,
+          // The caller's --show-toplevel is authoritative for its checkout.
+          // Keep this out of the snapshot shared with linked worktrees.
+          worktreePath: current ? repositoryPaths.worktreeRoot : ref.worktreePath,
+        };
+      });
       const combinedBranches = input.includeMatchingRemoteRefs
         ? [...localBranches, ...snapshot.remoteBranches]
         : dedupeRemoteBranchesWithLocalMatches([...localBranches, ...snapshot.remoteBranches]);