diff --git a/toolchain/driver/clang_subcommand.cpp b/toolchain/driver/clang_subcommand.cpp
index 75bc9bf994e0..2d1b89cc7867 100644
--- a/toolchain/driver/clang_subcommand.cpp
+++ b/toolchain/driver/clang_subcommand.cpp
@@ -44,6 +44,15 @@ Arguments passed to Clang.
 auto ClangSubcommand::Run(DriverEnv& driver_env) -> DriverResult {
   std::string target = llvm::sys::getDefaultTargetTriple();
   ClangRunner runner(driver_env.installation, target, driver_env.vlog_stream);
+
+  // Don't run Clang when fuzzing, it is known to not be reliable under fuzzing
+  // due to many unfixed issues.
+  if (driver_env.fuzzing) {
+    driver_env.error_stream
+        << "error: cannot run `clang` subcommand productively when fuzzing\n";
+    return {.success = false};
+  }
+
   return {.success = runner.Run(options_.args)};
 }
 
diff --git a/toolchain/driver/driver.cpp b/toolchain/driver/driver.cpp
index b1066b5e0036..508f15c63388 100644
--- a/toolchain/driver/driver.cpp
+++ b/toolchain/driver/driver.cpp
@@ -24,6 +24,7 @@ struct Options {
   auto Build(CommandLine::CommandBuilder& b) -> void;
 
   bool verbose;
+  bool fuzzing;
 
   ClangSubcommand clang;
   CompileSubcommand compile;
@@ -63,6 +64,13 @@ auto Options::Build(CommandLine::CommandBuilder& b) -> void {
       },
       [&](CommandLine::FlagBuilder& arg_b) { arg_b.Set(&verbose); });
 
+  b.AddFlag(
+      {
+          .name = "fuzzing",
+          .help = "Configure the command line for fuzzing.",
+      },
+      [&](CommandLine::FlagBuilder& arg_b) { arg_b.Set(&fuzzing); });
+
   b.AddSubcommand(ClangOptions::Info, [&](CommandLine::CommandBuilder& sub_b) {
     clang.BuildOptions(sub_b);
     sub_b.Do([&] { subcommand = &clang; });
@@ -109,8 +117,14 @@ auto Driver::RunCommand(llvm::ArrayRef<llvm::StringRef> args) -> DriverResult {
     // Note this implies streamed output in order to interleave.
     driver_env_.vlog_stream = &driver_env_.error_stream;
   }
+  if (options.fuzzing) {
+    SetFuzzing();
+  }
+
   CARBON_CHECK(options.subcommand != nullptr);
   return options.subcommand->Run(driver_env_);
 }
 
+auto Driver::SetFuzzing() -> void { driver_env_.fuzzing = true; }
+
 }  // namespace Carbon
diff --git a/toolchain/driver/driver.h b/toolchain/driver/driver.h
index 3a7315c914a7..5f3c65e9e082 100644
--- a/toolchain/driver/driver.h
+++ b/toolchain/driver/driver.h
@@ -38,6 +38,10 @@ class Driver {
   // error stream (stderr by default).
   auto RunCommand(llvm::ArrayRef<llvm::StringRef> args) -> DriverResult;
 
+  // Configure the driver for fuzzing. This allows specific commands to error
+  // rather than perform operations that aren't well behaved during fuzzing.
+  auto SetFuzzing() -> void;
+
  private:
   DriverEnv driver_env_;
 };
diff --git a/toolchain/driver/driver_env.h b/toolchain/driver/driver_env.h
index ad0966f8d9ad..03a8f36a5d97 100644
--- a/toolchain/driver/driver_env.h
+++ b/toolchain/driver/driver_env.h
@@ -25,6 +25,9 @@ struct DriverEnv {
 
   // For CARBON_VLOG.
   llvm::raw_pwrite_stream* vlog_stream = nullptr;
+
+  // Tracks when the driver is being fuzzed.
+  bool fuzzing = false;
 };
 
 }  // namespace Carbon
diff --git a/toolchain/driver/driver_fuzzer.cpp b/toolchain/driver/driver_fuzzer.cpp
index a5e145aea9a8..592ff2147a46 100644
--- a/toolchain/driver/driver_fuzzer.cpp
+++ b/toolchain/driver/driver_fuzzer.cpp
@@ -82,6 +82,7 @@ extern "C" auto LLVMFuzzerTestOneInput(const unsigned char* data, size_t size)
   TestRawOstream error_stream;
   llvm::raw_null_ostream dest;
   Driver d(fs, install_paths, dest, error_stream);
+  d.SetFuzzing();
   if (!d.RunCommand(args).success) {
     auto str = error_stream.TakeStr();
     // TODO: Fix command_line to use `error`, switch back to `find`.