diff --git a/agent/agent_init.py b/agent/agent_init.py
index 7539d59d35d..b3b499a9934 100644
--- a/agent/agent_init.py
+++ b/agent/agent_init.py
@@ -1822,6 +1822,8 @@ def init_agent(
         working_dir=os.getenv("TERMINAL_CWD") or None,
     )
     agent._user_turn_count = 0
+    # Copilot x-initiator flag: first API call of a user turn sends "user" (#3040).
+    agent._is_user_initiated_turn = False
 
     # Cumulative token usage for the session
     agent.session_prompt_tokens = 0
diff --git a/agent/conversation_loop.py b/agent/conversation_loop.py
index 41a13f5d628..dff11c489b5 100644
--- a/agent/conversation_loop.py
+++ b/agent/conversation_loop.py
@@ -1158,6 +1158,14 @@ def run_conversation(
                     _sanitize_structure_non_ascii(api_kwargs)
                 if agent.api_mode == "codex_responses":
                     api_kwargs = agent._get_transport().preflight_kwargs(api_kwargs, allow_stream=False)
+                # Copilot x-initiator: the first API call of a user turn is
+                # marked "user" so Copilot bills a premium request; tool-loop
+                # follow-ups keep the default "agent" header (#3040).
+                if getattr(agent, "_is_user_initiated_turn", False) and agent._is_copilot_url():
+                    _xh = dict(api_kwargs.get("extra_headers") or {})
+                    _xh["x-initiator"] = "user"
+                    api_kwargs["extra_headers"] = _xh
+                    agent._is_user_initiated_turn = False
                 try:
                     from hermes_cli.middleware import apply_llm_request_middleware
 
diff --git a/agent/turn_context.py b/agent/turn_context.py
index 88980b4ad27..f7951666d7e 100644
--- a/agent/turn_context.py
+++ b/agent/turn_context.py
@@ -277,6 +277,9 @@ def build_turn_context(
 
     # Track user turns for memory flush and periodic nudge logic.
     agent._user_turn_count += 1
+    # Copilot x-initiator: the first API call of this user turn is
+    # user-initiated; tool-loop follow-ups revert to "agent" (#3040).
+    agent._is_user_initiated_turn = True
 
     # Reset the streaming context scrubber at the top of each turn.
     scrubber = getattr(agent, "_stream_context_scrubber", None)
diff --git a/hermes_cli/models.py b/hermes_cli/models.py
index b9b5fc69967..f8ddf1ab33c 100644
--- a/hermes_cli/models.py
+++ b/hermes_cli/models.py
@@ -2783,7 +2783,7 @@ def _payload_items(payload: Any) -> list[dict[str, Any]]:
     return []
 
 
-def copilot_default_headers() -> dict[str, str]:
+def copilot_default_headers(*, is_agent_turn: bool = True) -> dict[str, str]:
     """Standard headers for Copilot API requests.
 
     Includes Openai-Intent and x-initiator headers that opencode and the
@@ -2791,13 +2791,13 @@ def copilot_default_headers() -> dict[str, str]:
     """
     try:
         from hermes_cli.copilot_auth import copilot_request_headers
-        return copilot_request_headers(is_agent_turn=True)
+        return copilot_request_headers(is_agent_turn=is_agent_turn)
     except ImportError:
         return {
             "Editor-Version": COPILOT_EDITOR_VERSION,
             "User-Agent": "HermesAgent/1.0",
             "Openai-Intent": "conversation-edits",
-            "x-initiator": "agent",
+            "x-initiator": "agent" if is_agent_turn else "user",
         }
 
 
diff --git a/run_agent.py b/run_agent.py
index cdd82f459c8..3cd458cd505 100644
--- a/run_agent.py
+++ b/run_agent.py
@@ -735,6 +735,10 @@ class AIAgent:
         # Turn counter (added after reset_session_state was first written — #2635)
         self._user_turn_count = 0
 
+        # Copilot x-initiator: True for the first API call of a user turn,
+        # False for tool-loop follow-ups (#3040).
+        self._is_user_initiated_turn = False
+
         # Context engine reset/transition (works for built-in compressor and plugins)
         self._transition_context_engine_session(
             old_session_id=old_session_id,
@@ -1327,6 +1331,13 @@ class AIAgent:
         """Return True when the base URL targets OpenRouter."""
         return base_url_host_matches(self._base_url_lower, "openrouter.ai")
 
+    def _is_copilot_url(self) -> bool:
+        """Return True when the base URL targets GitHub Copilot or GitHub Models."""
+        return (
+            "api.githubcopilot.com" in self._base_url_lower
+            or "models.github.ai" in self._base_url_lower
+        )
+
     def _anthropic_prompt_cache_policy(
         self,
         *,
diff --git a/scripts/release.py b/scripts/release.py
index baf873fe87d..058d9fb29e5 100755
--- a/scripts/release.py
+++ b/scripts/release.py
@@ -45,6 +45,8 @@ ACP_REGISTRY_MANIFEST = REPO_ROOT / "acp_registry" / "agent.json"
 
 # Auto-extracted from noreply emails + manual overrides
 AUTHOR_MAP = {
+    "tim@iteachyouai.com": "tjp2021",  # PR #4097 salvage (copilot: per-turn x-initiator header so user prompts bill as premium requests; #3040)
+    "3723267+kevinrajaram@users.noreply.github.com": "kevinrajaram",  # PR #3850 salvage (gateway: add POSIX system dirs to PATH so launchctl/systemctl resolve under UV's minimal-PATH bundled Python; #3849)
     "jonathan@mintrx.com": "JAlmanzarMint",  # PR #52688 salvage (vision: rasterize SVG / re-encode unsupported raster formats to PNG before embedding), folded into #57890
     "al3060388206@gmail.com": "ooiuuii",  # PR #58466/#58377 salvage (redact: fireworks fw-/fpk_ prefixes; telegram: redact bot tokens out of transport error strings). Also PR #58433 salvage (codex: accept recorded final_text when app-server omits turn/completed) and PR #58472 salvage (gateway: cap proxy SSE line buffer at 16MiB).
     "Jigoooo@users.noreply.github.com": "Jigoooo",  # PR #58474 salvage (auxiliary: fall back to token resolver when anthropic pool has no usable entry)
diff --git a/tests/hermes_cli/test_copilot_auth.py b/tests/hermes_cli/test_copilot_auth.py
index 3d0b0bdeb72..b658584f302 100644
--- a/tests/hermes_cli/test_copilot_auth.py
+++ b/tests/hermes_cli/test_copilot_auth.py
@@ -152,6 +152,34 @@ class TestCopilotDefaultHeaders:
         headers = copilot_default_headers()
         assert "x-initiator" in headers
 
+    def test_default_is_agent_turn(self):
+        """Calling with no args preserves backward-compatible default (agent)."""
+        from hermes_cli.models import copilot_default_headers
+        headers = copilot_default_headers()
+        assert headers["x-initiator"] == "agent"
+
+    def test_user_turn_sets_user_initiator(self):
+        """Passing is_agent_turn=False sets x-initiator to 'user'."""
+        from hermes_cli.models import copilot_default_headers
+        headers = copilot_default_headers(is_agent_turn=False)
+        assert headers["x-initiator"] == "user"
+
+    def test_agent_turn_explicit(self):
+        """Explicitly passing is_agent_turn=True sets x-initiator to 'agent'."""
+        from hermes_cli.models import copilot_default_headers
+        headers = copilot_default_headers(is_agent_turn=True)
+        assert headers["x-initiator"] == "agent"
+
+    def test_param_passthrough_both_values(self):
+        """is_agent_turn param correctly maps to x-initiator for both True and False."""
+        from hermes_cli.models import copilot_default_headers
+        for is_agent, expected in [(True, "agent"), (False, "user")]:
+            headers = copilot_default_headers(is_agent_turn=is_agent)
+            assert headers["x-initiator"] == expected, (
+                f"is_agent_turn={is_agent} should produce x-initiator={expected!r}, "
+                f"got {headers['x-initiator']!r}"
+            )
+
 
 class TestApiModeSelection:
     """API mode selection matching opencode's shouldUseCopilotResponsesApi."""
diff --git a/tests/test_copilot_initiator.py b/tests/test_copilot_initiator.py
new file mode 100644
index 00000000000..aa2915d0225
--- /dev/null
+++ b/tests/test_copilot_initiator.py
@@ -0,0 +1,148 @@
+"""Tests for per-turn Copilot x-initiator header injection (issue #3040).
+
+Copilot bills "premium requests" only when a request is marked as
+user-initiated via the ``x-initiator: user`` header. Hermes previously sent
+``x-initiator: agent`` on every request (client-level default headers), so
+user prompts never consumed premium requests and were throttled as agent
+traffic. The fix marks the FIRST API call of each user turn as "user" and
+lets tool-loop follow-ups keep the "agent" default.
+
+Salvaged from PR #4097 (@tjp2021); adapted to the post-refactor layout
+(conversation_loop.py owns the injection site, the codex transport now
+accepts extra_headers).
+"""
+
+import pytest
+
+from run_agent import AIAgent
+
+
+def _tool_defs(*names):
+    return [
+        {"type": "function", "function": {"name": n, "description": n, "parameters": {}}}
+        for n in names
+    ]
+
+
+class _FakeOpenAI:
+    def __init__(self, **kw):
+        self.api_key = kw.get("api_key", "test")
+        self.base_url = kw.get("base_url", "http://test")
+
+    def close(self):
+        pass
+
+
+def _make_agent(monkeypatch, base_url, api_mode="chat_completions"):
+    """Create an AIAgent pointing at the given base_url."""
+    monkeypatch.setattr("run_agent.get_tool_definitions", lambda **kw: _tool_defs("web_search"))
+    monkeypatch.setattr("run_agent.check_toolset_requirements", lambda: {})
+    monkeypatch.setattr("run_agent.OpenAI", _FakeOpenAI)
+    return AIAgent(
+        api_key="test-key",
+        base_url=base_url,
+        provider="copilot" if "githubcopilot" in base_url else "openrouter",
+        api_mode=api_mode,
+        max_iterations=4,
+        quiet_mode=True,
+        skip_context_files=True,
+        skip_memory=True,
+    )
+
+
+def _inject(agent, api_kwargs):
+    """Mirror the injection block in agent/conversation_loop.py."""
+    if getattr(agent, "_is_user_initiated_turn", False) and agent._is_copilot_url():
+        _xh = dict(api_kwargs.get("extra_headers") or {})
+        _xh["x-initiator"] = "user"
+        api_kwargs["extra_headers"] = _xh
+        agent._is_user_initiated_turn = False
+    return api_kwargs
+
+
+class TestIsCopilotUrl:
+    """_is_copilot_url() detects GitHub Copilot endpoints."""
+
+    def test_standard_copilot_url(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://api.githubcopilot.com")
+        assert agent._is_copilot_url() is True
+
+    def test_copilot_url_with_path(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://api.githubcopilot.com/v1")
+        assert agent._is_copilot_url() is True
+
+    def test_github_models_url(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://models.github.ai/inference")
+        assert agent._is_copilot_url() is True
+
+    def test_openrouter_url(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://openrouter.ai/api/v1")
+        assert agent._is_copilot_url() is False
+
+    def test_case_insensitive(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://API.GITHUBCOPILOT.COM")
+        assert agent._is_copilot_url() is True
+
+
+class TestUserInitiatedTurnFlag:
+    """_is_user_initiated_turn lifecycle."""
+
+    def test_default_is_false(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://api.githubcopilot.com")
+        assert agent._is_user_initiated_turn is False
+
+    def test_reset_session_clears_flag(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://api.githubcopilot.com")
+        agent._is_user_initiated_turn = True
+        agent.reset_session_state()
+        assert agent._is_user_initiated_turn is False
+
+
+class TestFlagFlipOnInjection:
+    """Flag flips immediately on injection so tool-loop calls use 'agent'."""
+
+    def test_first_call_injects_user_initiator(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://api.githubcopilot.com")
+        agent._is_user_initiated_turn = True
+        kwargs = _inject(agent, {})
+        assert kwargs["extra_headers"] == {"x-initiator": "user"}
+        assert agent._is_user_initiated_turn is False
+
+    def test_second_call_has_no_injection(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://api.githubcopilot.com")
+        agent._is_user_initiated_turn = True
+        kwargs1 = _inject(agent, {})
+        kwargs2 = _inject(agent, {})
+        assert "extra_headers" in kwargs1
+        assert "extra_headers" not in kwargs2
+
+    def test_existing_extra_headers_preserved(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://api.githubcopilot.com")
+        agent._is_user_initiated_turn = True
+        kwargs = _inject(agent, {"extra_headers": {"x-custom": "1"}})
+        assert kwargs["extra_headers"]["x-custom"] == "1"
+        assert kwargs["extra_headers"]["x-initiator"] == "user"
+
+    def test_non_copilot_flag_not_flipped(self, monkeypatch):
+        agent = _make_agent(monkeypatch, "https://openrouter.ai/api/v1")
+        agent._is_user_initiated_turn = True
+        kwargs = _inject(agent, {})
+        assert "extra_headers" not in kwargs
+        # Flag unchanged — non-Copilot path doesn't touch it
+        assert agent._is_user_initiated_turn is True
+
+
+class TestHeaderValues:
+    """copilot_default_headers(is_agent_turn=...) sets x-initiator correctly."""
+
+    def test_default_is_agent(self):
+        from hermes_cli.models import copilot_default_headers
+        assert copilot_default_headers()["x-initiator"] == "agent"
+
+    def test_user_turn(self):
+        from hermes_cli.models import copilot_default_headers
+        assert copilot_default_headers(is_agent_turn=False)["x-initiator"] == "user"
+
+    def test_agent_turn_explicit(self):
+        from hermes_cli.models import copilot_default_headers
+        assert copilot_default_headers(is_agent_turn=True)["x-initiator"] == "agent"