diff --git a/CMakeLists.txt b/CMakeLists.txt
index 32032afb00e..6db5aedf3fb 100644
--- a/CMakeLists.txt
+++ b/CMakeLists.txt
@@ -561,16 +561,21 @@ else()
   set_property(DIRECTORY APPEND PROPERTY CMAKE_CONFIGURE_DEPENDS ${syscalls_subdirs_txt})
 endif()
 
-# SYSCALL_INCLUDE_DIRECTORY will include the directories that needs to be
-# searched for syscall declarations if CONFIG_APPLICATION_DEFINED_SYSCALL is set
+# syscall declarations are searched for in the SYSCALL_INCLUDE_DIRS
 if(CONFIG_APPLICATION_DEFINED_SYSCALL)
-  set(SYSCALL_INCLUDE_DIRECTORY --include ${APPLICATION_SOURCE_DIR})
+  list(APPEND SYSCALL_INCLUDE_DIRS ${APPLICATION_SOURCE_DIR})
 endif()
 
 if(CONFIG_ZTEST)
-  set(SYSCALL_ZTEST_DIRECTORY --include ${ZEPHYR_BASE}/subsys/testsuite/ztest/include)
+  list(APPEND SYSCALL_INCLUDE_DIRS ${ZEPHYR_BASE}/subsys/testsuite/ztest/include)
 endif()
 
+foreach(d ${SYSCALL_INCLUDE_DIRS})
+  list(APPEND parse_syscalls_include_args
+    --include ${d}
+    )
+endforeach()
+
 add_custom_command(
   OUTPUT
   ${syscalls_json}
@@ -578,8 +583,7 @@ add_custom_command(
   ${PYTHON_EXECUTABLE}
   ${ZEPHYR_BASE}/scripts/parse_syscalls.py
    --include          ${ZEPHYR_BASE}/include        # Read files from this dir
-  ${SYSCALL_INCLUDE_DIRECTORY}
-  ${SYSCALL_ZTEST_DIRECTORY}
+  ${parse_syscalls_include_args}                    # Read files from these dirs also
   --json-file        ${syscalls_json}              # Write this file
   DEPENDS ${syscalls_subdirs_trigger} ${PARSE_SYSCALLS_HEADER_DEPENDS}
   )
diff --git a/doc/reference/usermode/syscalls.rst b/doc/reference/usermode/syscalls.rst
index a1665248eb2..037fb7fbd00 100644
--- a/doc/reference/usermode/syscalls.rst
+++ b/doc/reference/usermode/syscalls.rst
@@ -26,8 +26,9 @@ Components
 
 All system calls have the following components:
 
-* A **C prototype** for the API, declared in some header under ``include/`` and
-  prefixed with :c:macro:`__syscall`.  This prototype is never implemented
+* A **C prototype** prefixed with :c:macro:`__syscall` for the API. It
+  will be declared in some header under ``include/`` or in another
+  ``SYSCALL_INCLUDE_DIRS`` directory. This prototype is never implemented
   manually, instead it gets created by the :ref:`gen_syscalls.py` script.
   What gets generated is an inline function which either calls the
   implementation function directly (if called from supervisor mode) or goes
@@ -88,6 +89,15 @@ bottom of ``include/sensor.h``:
 
     #include <syscalls/sensor.h>
 
+C prototype functions must be declared in one of the directories
+listed in the CMake variable ``SYSCALL_INCLUDE_DIRS``. This list
+always contains ``${ZEPHYR_BASE}/include``, but will also contain
+``APPLICATION_SOURCE_DIR`` when ``CONFIG_APPLICATION_DEFINED_SYSCALL``
+is set, or ``${ZEPHYR_BASE}/subsys/testsuite/ztest/include`` when
+``CONFIG_ZTEST`` is set. Additional paths can be added to the list
+through the CMake command line or in CMake code that is run before
+``${ZEPHYR_BASE}/cmake/app/boilerplate.cmake`` is run.
+
 Invocation Context
 ==================