diff --git a/src/C/regions.jl b/src/C/regions.jl
index 26af46fe..81b5747d 100644
--- a/src/C/regions.jl
+++ b/src/C/regions.jl
@@ -1,27 +1,83 @@
 const PyThreadStatePtr = Ptr{Cvoid}
 
-mutable struct ThreadState
-    sem::Base.Semaphore
-    tstate::PyThreadStatePtr
-end
-ThreadState() = ThreadState(Base.Semaphore(1), C_NULL)
-
 mutable struct TaskState
+    # CPython state used by this task for the duration of its outermost region.
     tstate::PyThreadStatePtr
+    # Semaphore protecting `tstate`; `nothing` when the task is outside a session.
     sem::Union{Nothing,Base.Semaphore}
+    # Whether `tstate` is currently attached to the task's pinned OS thread.
     attached::Bool
+    # Julia thread to which the task is pinned while its session is active.
     tid::Int
+    # Stickiness to restore when the task's outermost region or break finishes.
     oldsticky::Bool
 end
 TaskState() = TaskState(C_NULL, nothing, false, 0, false)
 
+mutable struct ThreadState
+    # Serializes tasks which use the persistent CPython state on this Julia thread.
+    sem::Base.Semaphore
+    # PythonCall-owned CPython state for this Julia thread, allocated lazily.
+    tstate::PyThreadStatePtr
+    # Task which currently holds `sem` with a CPython state attached, if any.
+    task::Union{Nothing,Task}
+    # State belonging to `task`; cached so nested regions need no task-local lookup.
+    task_state::Union{Nothing,TaskState}
+end
+ThreadState() = ThreadState(Base.Semaphore(1), C_NULL, nothing, nothing)
+
 const THREAD_STATE = Utils.OncePerThread{ThreadState}(ThreadState)
 const TASK_STATE = Utils.OncePerTask{TaskState}(TaskState)
 
+# A region session starts at the outermost region entered by a Julia task and ends
+# when that region exits. The task is made sticky for the whole session: CPython
+# thread states must be restored on the same OS thread on which they were saved.
+# The corresponding ThreadState semaphore gives the task exclusive use of that
+# thread's persistent PyThreadState. A Python-originated call already has a CPython
+# state attached; that state is borrowed instead, but is protected by the same
+# semaphore so PythonCall's accounting remains identical.
+#
+# Nested regions merely return `:noop`. A break saves/detaches the CPython state,
+# clears the thread cache, and releases the semaphore, allowing other sticky tasks
+# to use this Julia thread while the original task yields. On return it reacquires
+# the semaphore before restoring both the CPython state and cache. Consequently the
+# cache is populated exactly while a task owns the semaphore with Python attached.
+# This invariant is what makes its lock-free fast path safe.
+#
+# An attached CPython state is also a still cheaper fast path for @pyregion itself.
+# Given that PythonCall is the only Julia-side entry to Python, an attached state
+# means either that an enclosing region already did the bookkeeping or that Python
+# called into Julia and lent us its state. In either case a nested region has no
+# transition to perform. Conversely, a region inside a break observes no attached
+# state and takes the full path below, reacquiring and restoring its task state.
+
 current_tstate() = PyThreadState_GetUnchecked()
 has_tstate() = CTX.is_initialized && current_tstate() != C_NULL
 
+# An attached task is pinned to this Julia thread and owns its semaphore, so the
+# thread-local cache cannot change underneath it.  This makes nested regions avoid
+# the considerably more expensive OncePerTask lookup.  The cache is cleared before
+# releasing the semaphore and restored after reacquiring it around a region break.
+function current_task_state(task::Task)
+    ts = THREAD_STATE()
+    return ts.task === task ? ts.task_state::TaskState : TASK_STATE()
+end
+
+function set_task!(ts::ThreadState, task::Task, s::TaskState)
+    ts.task = task
+    ts.task_state = s
+    return
+end
+
+function clear_task!(ts::ThreadState)
+    ts.task = nothing
+    ts.task_state = nothing
+    return
+end
+
 function reset!(s::TaskState)
+    # `oldsticky` is deliberately left alone: start_session! overwrites it before
+    # the TaskState becomes observable as an active session again.
     s.tstate = C_NULL
     s.sem = nothing
     s.attached = false
@@ -30,6 +86,8 @@ function reset!(s::TaskState)
 end
 
 function start_session!(task::Task, s::TaskState)
+    # Pin before recording the thread and looking up its ThreadState. Once sticky,
+    # cooperative scheduling cannot resume this task on another Julia thread.
     s.oldsticky = task.sticky
     task.sticky = true
     s.tid = Threads.threadid()
@@ -45,6 +103,8 @@ end
 
 function enter_region(task::Task, s::TaskState)
     if s.tstate != C_NULL
+        # An existing session is either already attached (ordinary nesting), or
+        # temporarily detached because this region is nested inside a break.
         check_thread(task, s)
         if s.attached
             return :noop
@@ -53,6 +113,7 @@ function enter_region(task::Task, s::TaskState)
         try
             PyEval_RestoreThread(s.tstate)
             s.attached = true
+            set_task!(THREAD_STATE(), task, s)
         catch
             Base.release(s.sem::Base.Semaphore)
             rethrow()
@@ -73,8 +134,10 @@ function enter_region(task::Task, s::TaskState)
         acquired = true
         current = current_tstate()
         if current != C_NULL
+            # Calls originating in Python must return with its state still attached.
             s.tstate = current
             s.attached = true
+            set_task!(ts, task, s)
             return :root_borrowed
         end
         if ts.tstate == C_NULL
@@ -84,6 +147,7 @@ function enter_region(task::Task, s::TaskState)
         s.tstate = ts.tstate
         PyEval_RestoreThread(s.tstate)
         s.attached = true
+        set_task!(ts, task, s)
         return :root_owned
     catch
         acquired && Base.release(ts.sem)
@@ -94,23 +158,28 @@ function enter_region(task::Task, s::TaskState)
 end
 
 function exit_region(task::Task, s::TaskState, token)
+    # Tokens encode precisely which work enter_region performed, so every path
+    # reverses only its own transition and nested :noop regions do no attach work.
     token === :noop && return
     check_thread(task, s)
     if token === :detach
         saved = PyEval_SaveThread()
         @assert saved == s.tstate
         s.attached = false
+        clear_task!(THREAD_STATE())
         Base.release(s.sem::Base.Semaphore)
     elseif token === :root_owned
         saved = PyEval_SaveThread()
         @assert saved == s.tstate
         sem, oldsticky = s.sem::Base.Semaphore, s.oldsticky
+        clear_task!(THREAD_STATE())
         reset!(s)
         Base.release(sem)
         task.sticky = oldsticky
     elseif token === :root_borrowed
         @assert current_tstate() == s.tstate
         sem, oldsticky = s.sem::Base.Semaphore, s.oldsticky
+        clear_task!(THREAD_STATE())
         reset!(s)
         Base.release(sem)
         task.sticky = oldsticky
@@ -122,14 +191,18 @@ end
 
 function enter_break(task::Task, s::TaskState)
     if s.tstate != C_NULL
+        # Only the outermost break detaches. Further breaks while detached are no-ops.
         check_thread(task, s)
         !s.attached && return :noop
         saved = PyEval_SaveThread()
         @assert saved == s.tstate
         s.attached = false
+        clear_task!(THREAD_STATE())
         Base.release(s.sem::Base.Semaphore)
         return :restore
     end
+    # Outside a region, a break matters only in a Python-originated callback. It
+    # borrows and detaches that state so yielding Julia code cannot retain Python.
     current_tstate() == C_NULL && return :noop
 
     ts = try
@@ -170,8 +243,12 @@ function exit_break(task::Task, s::TaskState, token)
     Base.acquire(s.sem::Base.Semaphore)
     PyEval_RestoreThread(s.tstate)
     s.attached = true
+    set_task!(THREAD_STATE(), task, s)
     if token === :root_restore
+        # The borrowed Python state stays attached for the caller, but the temporary
+        # Julia session and its cache ownership end here.
         sem, oldsticky = s.sem::Base.Semaphore, s.oldsticky
+        clear_task!(THREAD_STATE())
         reset!(s)
         Base.release(sem)
         task.sticky = oldsticky
@@ -191,13 +268,19 @@ blocks cooperatively in [`@pyregionbreak`](@ref).
 """
 macro pyregion(ex)
     quote
-        local task = current_task()
-        local state = $TASK_STATE()
-        local token = $enter_region(task, state)
-        try
+        if $current_tstate() != C_NULL
+            # The CPython TLS lookup is enough to prove that this region is nested
+            # or Python-originated; avoid both Julia task- and thread-local lookups.
             $(esc(ex))
-        finally
-            $exit_region(task, state, token)
+        else
+            local task = current_task()
+            local state = $current_task_state(task)
+            local token = $enter_region(task, state)
+            try
+                $(esc(ex))
+            finally
+                $exit_region(task, state, token)
+            end
         end
     end
 end
@@ -212,7 +295,7 @@ PythonCall operations still work automatically, and both kinds of region nest fr
 macro pyregionbreak(ex)
     quote
         local task = current_task()
-        local state = $TASK_STATE()
+        local state = $current_task_state(task)
         local token = $enter_break(task, state)
         try
             $(esc(ex))
diff --git a/test/C.jl b/test/C.jl
index 69f8697a..c1ffdded 100644
--- a/test/C.jl
+++ b/test/C.jl
@@ -16,3 +16,61 @@
         @test PythonCall.python_version().major == 3
     end
 end
+
+@testitem "Python regions and task-safe thread states" setup = [Setup] begin
+    using Base.Threads
+
+    @test PythonCall.C.PyThreadState_GetUnchecked() == C_NULL
+    @test @pyregion pyconvert(Int, pyint(12)) == 12
+    @test PythonCall.C.PyThreadState_GetUnchecked() == C_NULL
+
+    # Nested regions reuse the state cached by the owning Julia thread. A break
+    # must relinquish that cache while yielding and restore it on return.
+    @pyregion begin
+        local state = PythonCall.C.TASK_STATE()
+        local thread_state = PythonCall.C.THREAD_STATE()
+        @test thread_state.task === current_task()
+        @test thread_state.task_state === state
+        @pyregion @test PythonCall.C.current_task_state(current_task()) === state
+        @pyregionbreak begin
+            @test thread_state.task === nothing
+            yield()
+        end
+        @test thread_state.task === current_task()
+        @test thread_state.task_state === state
+    end
+    @test PythonCall.C.THREAD_STATE().task === nothing
+
+    @test @pyregion begin
+        @pyregion pyconvert(Int, pyint(1)) == 1
+        @pyregionbreak begin
+            yield()
+            @pyregion pyconvert(Int, pyint(2)) == 2
+            @pyregionbreak yield()
+        end
+        pyconvert(Int, pyint(3)) == 3
+    end
+
+    @test_throws ErrorException @pyregion @pyregionbreak error("region exception")
+    @test PythonCall.C.PyThreadState_GetUnchecked() == C_NULL
+    @test_throws PyException @pyregion pybuiltins.int("not an integer")
+    @test pyconvert(Int, pyint(5)) == 5
+
+    results = fetch.([@spawn begin
+        total = 0
+        for i in 1:100
+            total += pyconvert(Int, pyint(i))
+            @pyregionbreak yield()
+        end
+        total
+    end for _ in 1:max(8, 2nthreads())])
+    @test all(==(5050), results)
+
+    f = pyfunc() do
+        yield()
+        pyconvert(Int, pybuiltins.sum([1, 2, 3]))
+    end
+    @test pyconvert(Int, f()) == 6
+
+    @test pyconvert(Int, @py 1 + @jl(pyconvert(Int, pyint(2)))) == 3
+end
diff --git a/test/Region.jl b/test/Region.jl
deleted file mode 100644
index b000ad52..00000000
--- a/test/Region.jl
+++ /dev/null
@@ -1,42 +0,0 @@
-using TestItemRunner
-
-@testitem "Python regions and task-safe thread states" setup = [Setup] begin
-    using Base.Threads
-
-    @test PythonCall.C.PyThreadState_GetUnchecked() == C_NULL
-    @test @pyregion pyconvert(Int, pyint(12)) == 12
-    @test PythonCall.C.PyThreadState_GetUnchecked() == C_NULL
-
-    @test @pyregion begin
-        @pyregion pyconvert(Int, pyint(1)) == 1
-        @pyregionbreak begin
-            yield()
-            @pyregion pyconvert(Int, pyint(2)) == 2
-            @pyregionbreak yield()
-        end
-        pyconvert(Int, pyint(3)) == 3
-    end
-
-    @test_throws ErrorException @pyregion @pyregionbreak error("region exception")
-    @test PythonCall.C.PyThreadState_GetUnchecked() == C_NULL
-    @test_throws PyException @pyregion pybuiltins.int("not an integer")
-    @test pyconvert(Int, pyint(5)) == 5
-
-    results = fetch.([@spawn begin
-        total = 0
-        for i in 1:100
-            total += pyconvert(Int, pyint(i))
-            @pyregionbreak yield()
-        end
-        total
-    end for _ in 1:max(8, 2nthreads())])
-    @test all(==(5050), results)
-
-    f = pyfunc() do
-        yield()
-        pyconvert(Int, pybuiltins.sum([1, 2, 3]))
-    end
-    @test pyconvert(Int, f()) == 6
-
-    @test pyconvert(Int, @py 1 + @jl(pyconvert(Int, pyint(2)))) == 3
-end