diff --git a/backend/apps/agents/manager/configure_provider_env.py b/backend/apps/agents/manager/configure_provider_env.py
index c98ea304..bc4ce34c 100644
--- a/backend/apps/agents/manager/configure_provider_env.py
+++ b/backend/apps/agents/manager/configure_provider_env.py
@@ -241,6 +241,17 @@ async def configure_provider_env(
                 "with a direct API key."
             )
         raise ValueError("No AI provider configured. Set an API key or connect a subscription.")
+    # ENABLE_TOOL_SEARCH belongs to EVERY lane, so it is set after the branch chain rather than
+    # inside it. The CLI's tengu_defer_all_bn4 defers every tool, which collides with cache_control
+    # and 400s the next tool-laden request ("cannot have both defer_loading=true and cache_control
+    # set", ENG-394). That collision is CLI-side and has nothing to do with which credential pays,
+    # yet the flag was set in 4 of 8 branches; the direct-Anthropic-key lanes were among the misses,
+    # which is exactly where it was hit on opus-5. A default applied inside a branch protects only
+    # that branch, and the next branch added forgets it again.
+    p_env = options_kwargs.get("env")
+    if isinstance(p_env, dict):
+        p_env.setdefault("ENABLE_TOOL_SEARCH", "auto")
+
     # Fault-injection seam: lets a QA harness front the provider with a local proxy (mid-run 401 drills, ENG-302 family). Absent in prod, so every branch's real base URL stands.
     p_base_override = os.environ.get("OPENSWARM_ANTHROPIC_BASE_OVERRIDE")
     if p_base_override and isinstance(options_kwargs.get("env"), dict):
diff --git a/backend/tests/test_tool_search_flag_every_lane.py b/backend/tests/test_tool_search_flag_every_lane.py
new file mode 100644
index 00000000..0fd04fe2
--- /dev/null
+++ b/backend/tests/test_tool_search_flag_every_lane.py
@@ -0,0 +1,60 @@
+"""Every provider lane sets ENABLE_TOOL_SEARCH, because the collision it prevents is CLI-side.
+
+ENG-394: a ToolSearch-deferred tool 400s the NEXT request with "cannot have both
+defer_loading=true and cache_control set". The CLI's `tengu_defer_all_bn4` defers every tool;
+`ENABLE_TOOL_SEARCH=auto` stops it. That was already known and already fixed -- in 4 of 8 branches.
+The direct-Anthropic-key lanes were among the four misses, which is precisely where it was hit on
+opus-5, and it later killed a user's app build mid-flight.
+
+Same defect this codebase keeps paying for: a guard inside one branch protects only that branch,
+and the next branch added forgets it. The flag is now applied AFTER the chain, where no branch can
+miss it.
+"""
+
+import re
+
+SRC = "backend/apps/agents/manager/configure_provider_env.py"
+
+
+def p_src() -> str:
+    return open(SRC).read()
+
+
+def test_the_flag_is_applied_outside_the_branch_chain():
+    src = p_src()
+    i = src.index('p_env.setdefault("ENABLE_TOOL_SEARCH", "auto")')
+    # Everything before it in the function is the if/elif chain; the setdefault must come after the
+    # LAST elif, so no branch can return without it.
+    last_elif = src.rindex("\n    elif ", 0, i)
+    assert last_elif < i, "it must sit below every branch, not inside one"
+
+
+def test_it_never_overrides_a_branch_that_set_it_deliberately():
+    src = p_src()
+    assert "setdefault(" in src, "a branch with its own value keeps it"
+    assert 'p_env["ENABLE_TOOL_SEARCH"] =' not in src
+
+
+def test_it_survives_a_branch_that_ships_only_one_key():
+    """The direct-api-key lane is literally `{"ANTHROPIC_API_KEY": ...}`; that is the shape that
+    was missing the flag, and the same shape the base-override seam already had to be fixed for."""
+    src = p_src()
+    assert '{"ANTHROPIC_API_KEY": global_settings.anthropic_api_key}' in src
+    i = src.index('{"ANTHROPIC_API_KEY": global_settings.anthropic_api_key}')
+    j = src.index('p_env.setdefault("ENABLE_TOOL_SEARCH", "auto")')
+    assert i < j, "the setdefault runs after that branch assigns its env"
+
+
+def test_a_lane_with_no_env_at_all_does_not_crash():
+    src = p_src()
+    i = src.index('p_env = options_kwargs.get("env")')
+    assert "isinstance(p_env, dict)" in src[i:i + 200], \
+        "a branch that never set env must not raise on the way past"
+
+
+def test_no_branch_quietly_disables_deferral_some_other_way():
+    # If a lane ever needs deferral ON, it must say so explicitly rather than by omission, which is
+    # how this got lost the first time.
+    src = p_src()
+    for m in re.finditer(r'ENABLE_TOOL_SEARCH["\']\s*[:=]\s*["\']([a-z]+)["\']', src):
+        assert m.group(1) == "auto", f"unexpected ENABLE_TOOL_SEARCH value {m.group(1)!r}"