diff --git a/.bazelci/presubmit.yml b/.bazelci/presubmit.yml
index e95a173c5b..d8e0b6eabc 100644
--- a/.bazelci/presubmit.yml
+++ b/.bazelci/presubmit.yml
@@ -92,8 +92,10 @@ tasks:
     test_targets: *default_linux_targets
     build_flags:
       - "--compilation_mode=opt"
+      - "--@rules_rust//rust/settings:experimental_toolchain_generated_sysroot=True"
     test_flags:
       - "--compilation_mode=opt"
+      - "--@rules_rust//rust/settings:experimental_toolchain_generated_sysroot=True"
   macos_opt:
     name: Opt Mode
     platform: macos
diff --git a/rust/private/rustdoc.bzl b/rust/private/rustdoc.bzl
index 1859c4aa3a..5fa82b8144 100644
--- a/rust/private/rustdoc.bzl
+++ b/rust/private/rustdoc.bzl
@@ -137,10 +137,6 @@ def rustdoc_compile_action(
         if "OUT_DIR" in env:
             env.update({"OUT_DIR": "${{pwd}}/{}".format(build_info.out_dir.short_path)})
 
-        # `rustdoc` does not support the SYSROOT environment variable. To account
-        # for this, the flag must be explicitly passed to the `rustdoc` binary.
-        args.rustc_flags.add(toolchain.sysroot_short_path, format = "--sysroot=${{pwd}}/%s")
-
     return struct(
         executable = ctx.executable._process_wrapper,
         inputs = depset([crate_info.output], transitive = [compile_inputs]),
diff --git a/rust/settings/BUILD.bazel b/rust/settings/BUILD.bazel
index 0cf1253831..a86bb149bf 100644
--- a/rust/settings/BUILD.bazel
+++ b/rust/settings/BUILD.bazel
@@ -1,5 +1,6 @@
 load("@bazel_skylib//:bzl_library.bzl", "bzl_library")
 load("@bazel_skylib//rules:common_settings.bzl", "bool_flag", "string_flag")
+load(":incompatible.bzl", "incompatible_flag")
 
 package(default_visibility = ["//visibility:public"])
 
@@ -63,3 +64,10 @@ bzl_library(
     name = "bzl_lib",
     srcs = glob(["**/*.bzl"]),
 )
+
+# A flag to set rustc --sysroot flag to the sysroot generated by rust_toolchain
+incompatible_flag(
+    name = "experimental_toolchain_generated_sysroot",
+    build_setting_default = False,
+    issue = "https://github.com/bazelbuild/rules_rust/issues/2039",
+)
diff --git a/rust/toolchain.bzl b/rust/toolchain.bzl
index 3a59d49d73..bc00ce3450 100644
--- a/rust/toolchain.bzl
+++ b/rust/toolchain.bzl
@@ -16,6 +16,7 @@ load(
     "find_cc_toolchain",
     "make_static_lib_symlink",
 )
+load("//rust/settings:incompatible.bzl", "IncompatibleFlagInfo")
 
 rust_analyzer_toolchain = _rust_analyzer_toolchain
 rustfmt_toolchain = _rustfmt_toolchain
@@ -537,6 +538,12 @@ def _rust_toolchain_impl(ctx):
     sysroot_path = sysroot.sysroot_anchor.dirname
     sysroot_short_path, _, _ = sysroot.sysroot_anchor.short_path.rpartition("/")
 
+    # Override "rustc --print sysroot" with sysroot generated by `_generate_sysroot`
+    # in this rule implementation
+    rustc_flags = ctx.attr.extra_rustc_flags
+    if ctx.attr._experimental_toolchain_generated_sysroot[IncompatibleFlagInfo].enabled == True:
+        rustc_flags = ["--sysroot=" + sysroot_path] + rustc_flags
+
     # Variables for make variable expansion
     make_variables = {
         "RUSTC": sysroot.rustc.path,
@@ -623,7 +630,7 @@ def _rust_toolchain_impl(ctx):
         rustfmt = sysroot.rustfmt,
         staticlib_ext = ctx.attr.staticlib_ext,
         stdlib_linkflags = stdlib_linkflags_cc_info,
-        extra_rustc_flags = ctx.attr.extra_rustc_flags,
+        extra_rustc_flags = rustc_flags,
         extra_exec_rustc_flags = ctx.attr.extra_exec_rustc_flags,
         per_crate_rustc_flags = ctx.attr.per_crate_rustc_flags,
         sysroot = sysroot_path,
@@ -787,6 +794,13 @@ rust_toolchain = rule(
         "_cc_toolchain": attr.label(
             default = Label("@bazel_tools//tools/cpp:current_cc_toolchain"),
         ),
+        "_experimental_toolchain_generated_sysroot": attr.label(
+            default = Label("//rust/settings:experimental_toolchain_generated_sysroot"),
+            doc = (
+                "Label to a boolean build setting that lets the rule knows wheter to set --sysroot to rustc" +
+                "This flag is only relevant when used together with --@rules_rust//rust/settings:experimental_toolchain_generated_sysroot."
+            ),
+        ),
         "_experimental_use_coverage_metadata_files": attr.label(
             default = Label("//rust/settings:experimental_use_coverage_metadata_files"),
         ),
diff --git a/test/toolchain/toolchain_test.bzl b/test/toolchain/toolchain_test.bzl
index cfa429ebbf..5c74fae6d1 100644
--- a/test/toolchain/toolchain_test.bzl
+++ b/test/toolchain/toolchain_test.bzl
@@ -36,12 +36,23 @@ def _toolchain_adds_rustc_flags_impl(ctx):
         "Found exec toolchain flag ({}) in rustc flags: {}".format(EXEC_TOOLCHAIN_FLAG, action.argv),
     )
 
+    found_sysroot = False
+    for arg in action.argv:
+        if arg.startswith("--sysroot") and arg.endswith("test/toolchain/rust_extra_flags_toolchain"):
+            found_sysroot = True
+    asserts.true(
+        env,
+        found_sysroot,
+        "Missing --sysroot flag or --sysroot does not point to correct sysroot directory",
+    )
+
     return analysistest.end(env)
 
 toolchain_adds_rustc_flags_test = analysistest.make(
     _toolchain_adds_rustc_flags_impl,
     config_settings = {
         str(Label("//:extra_rustc_flags")): [CONFIG_FLAG],
+        str(Label("//rust/settings:experimental_toolchain_generated_sysroot")): True,
     },
 )