diff --git a/esphome/components/api/api_pb2.h b/esphome/components/api/api_pb2.h
index 45d5f673f6..c2675cefe4 100644
--- a/esphome/components/api/api_pb2.h
+++ b/esphome/components/api/api_pb2.h
@@ -2,10 +2,6 @@
 // See script/api_protobuf/api_protobuf.py
 #pragma once
 
-#include "esphome/core/defines.h"
-#ifdef USE_BLUETOOTH_PROXY
-#define USE_API_VARINT64
-#endif
 #include "esphome/core/string_ref.h"
 
 #include "proto.h"
diff --git a/esphome/components/api/api_pb2_defines.h b/esphome/components/api/api_pb2_defines.h
new file mode 100644
index 0000000000..8ebd60fb5d
--- /dev/null
+++ b/esphome/components/api/api_pb2_defines.h
@@ -0,0 +1,12 @@
+// This file was automatically generated with a tool.
+// See script/api_protobuf/api_protobuf.py
+#pragma once
+
+#include "esphome/core/defines.h"
+#ifdef USE_BLUETOOTH_PROXY
+#ifndef USE_API_VARINT64
+#define USE_API_VARINT64
+#endif
+#endif
+
+namespace esphome::api {}  // namespace esphome::api
diff --git a/esphome/components/api/proto.h b/esphome/components/api/proto.h
index cbafccb80c..c34f7744e6 100644
--- a/esphome/components/api/proto.h
+++ b/esphome/components/api/proto.h
@@ -1,5 +1,6 @@
 #pragma once
 
+#include "api_pb2_defines.h"
 #include "esphome/core/component.h"
 #include "esphome/core/helpers.h"
 #include "esphome/core/log.h"
@@ -118,7 +119,7 @@ class ProtoVarInt {
     }
     // 32-bit phase: process remaining bytes with native 32-bit shifts.
     // Without USE_API_VARINT64: cover bytes 1-4 (shifts 7, 14, 21, 28) — the uint32_t
-    // shift at byte 4 truncates upper bits but those are always zero for valid uint32 values.
+    // shift at byte 4 (shift by 28) may lose bits 32-34, but those are always zero for valid uint32 values.
     // With USE_API_VARINT64: cover bytes 1-3 (shifts 7, 14, 21) so parse_wide handles
     // byte 4+ with full 64-bit arithmetic (avoids truncating values > UINT32_MAX).
     uint32_t result32 = buffer[0] & 0x7F;
diff --git a/script/api_protobuf/api_protobuf.py b/script/api_protobuf/api_protobuf.py
index 9b2bdb08c8..350947a8d6 100755
--- a/script/api_protobuf/api_protobuf.py
+++ b/script/api_protobuf/api_protobuf.py
@@ -1937,6 +1937,9 @@ def get_varint64_ifdef(
     }
     if not ifdefs:
         return False, None
+    if None in ifdefs:
+        # At least one 64-bit varint field is unconditional, so the guard must be unconditional.
+        return True, None
     ifdefs.discard(None)
     return True, ifdefs.pop() if len(ifdefs) == 1 else None
 
@@ -2601,22 +2604,32 @@ def main() -> None:
     )
 
     # Find the ifdef guard for 64-bit varint fields (int64/uint64/sint64).
-    # Emitted before proto.h so parse_wide_() and 64-bit accessors are available.
+    # Generated into api_pb2_defines.h so proto.h can include it, ensuring
+    # consistent ProtoVarInt layout across all translation units.
     has_varint64, varint64_guard = get_varint64_ifdef(file, message_ifdef_map)
 
+    # Generate api_pb2_defines.h — included by proto.h to ensure all translation
+    # units see USE_API_VARINT64 consistently (avoids ODR violations in ProtoVarInt).
+    defines_content = FILE_HEADER
+    defines_content += "#pragma once\n\n"
+    defines_content += '#include "esphome/core/defines.h"\n'
+    if has_varint64:
+        lines = [
+            "#ifndef USE_API_VARINT64",
+            "#define USE_API_VARINT64",
+            "#endif",
+        ]
+        defines_content += "\n".join(wrap_with_ifdef(lines, varint64_guard))
+        defines_content += "\n"
+    defines_content += "\nnamespace esphome::api {}  // namespace esphome::api\n"
+
+    with open(root / "api_pb2_defines.h", "w", encoding="utf-8") as f:
+        f.write(defines_content)
+
     content = FILE_HEADER
     content += """\
 #pragma once
 
-#include "esphome/core/defines.h"
-"""
-    if has_varint64:
-        content += "\n".join(
-            wrap_with_ifdef(["#define USE_API_VARINT64"], varint64_guard)
-        )
-        content += "\n"
-
-    content += """\
 #include "esphome/core/string_ref.h"
 
 #include "proto.h"