diff --git a/core/base/CMakeLists.txt b/core/base/CMakeLists.txt
index 35d1d3a42d3bb..e3b6159943813 100644
--- a/core/base/CMakeLists.txt
+++ b/core/base/CMakeLists.txt
@@ -233,15 +233,19 @@ set(full_core_filename $<TARGET_FILE_NAME:Core>)
 # Absolue CMAKE_INSTALL_<dir> paths are discouraged in CMake, but some
 # packagers use them anyway. So we support it.
 if(IS_ABSOLUTE ${CMAKE_INSTALL_INCLUDEDIR})
-   set(install_includedir_is_absolute 1)
+  set(install_lib_to_include "${CMAKE_INSTALL_INCLUDEDIR}")
 else()
-   set(install_includedir_is_absolute 0)
+  if(IS_ABSOLUTE ${CMAKE_INSTALL_LIBDIR})
+    set(libdir "${CMAKE_INSTALL_LIBDIR}")
+  else()
+    set(libdir "${CMAKE_INSTALL_PREFIX}/${CMAKE_INSTALL_LIBDIR}")
+  endif()
+  file(RELATIVE_PATH install_lib_to_include "${libdir}" "${CMAKE_INSTALL_PREFIX}/${CMAKE_INSTALL_INCLUDEDIR}")
+  unset(libdir)
 endif()
-file(TO_NATIVE_PATH "${CMAKE_INSTALL_INCLUDEDIR}" install_includedir_native)
 
 target_compile_options(Core PRIVATE -DLIB_CORE_NAME=${full_core_filename}
-                                    -DINSTALL_INCLUDEDIR=${install_includedir_native}
-                                    -DINSTALL_INCLUDEDIR_IS_ABSOLUTE=${install_includedir_is_absolute}
+                                    -DINSTALL_LIB_TO_INCLUDE="${install_lib_to_include}"
 )
 add_dependencies(Core ensure_build_tree_marker)
 
diff --git a/core/base/src/TROOT.cxx b/core/base/src/TROOT.cxx
index 9a58378ebea58..a9d9bb5cdc189 100644
--- a/core/base/src/TROOT.cxx
+++ b/core/base/src/TROOT.cxx
@@ -3182,21 +3182,27 @@ const TString &TROOT::GetIncludeDir()
    if (!rootincdir.IsNull())
       return rootincdir;
 
-   const std::string &sep = ROOT::FoundationUtils::GetPathSeparator();
+   namespace fs = std::filesystem;
+
+   // The shared library directory can be found automatically, because the
+   // libCore is loaded by definition when using TROOT. It's used as the anchor
+   // to resolve the ROOT include directory, using the correct relative path
+   // for either the build or install tree.
+   fs::path libPath = GetSharedLibDir().Data();
 
    // Check if we are in the build tree using the build tree marker file
-   const bool isBuildTree = std::filesystem::exists((GetSharedLibDir() + sep + "root-build-tree-marker").Data());
+   const bool isBuildTree = fs::exists(libPath / "root-build-tree-marker");
 
-   if (isBuildTree) {
-      rootincdir = GetRootSys() + sep + "include";
-   } else {
-#if INSTALL_INCLUDEDIR_IS_ABSOLUTE
-      rootincdir = _R_QUOTEVAL_(INSTALL_INCLUDEDIR);
-#else
-      rootincdir = GetRootSys() + sep + _R_QUOTEVAL_(INSTALL_INCLUDEDIR);
-#endif
+   fs::path includePath = isBuildTree ? "../include" : INSTALL_LIB_TO_INCLUDE;
+
+   // The INSTALL_LIB_TO_INCLUDE might already be absolute
+   if (!includePath.is_absolute()) {
+      includePath = libPath / includePath;
    }
 
+   // Normalize to get rid of the "../" in relative paths
+   rootincdir = includePath.lexically_normal().string();
+
    return rootincdir;
 }
 
diff --git a/core/base/test/CMakeLists.txt b/core/base/test/CMakeLists.txt
index e839d78255c9f..291d4399cbf87 100644
--- a/core/base/test/CMakeLists.txt
+++ b/core/base/test/CMakeLists.txt
@@ -20,6 +20,7 @@ if(ROOT_NEED_STDCXXFS)
     target_link_libraries(CoreBaseTests PRIVATE stdc++fs)
 endif()
 target_compile_options(CoreBaseTests PRIVATE -DEXPECTED_SHARED_LIBRARY_DIR="${localruntimedir}")
+target_compile_options(CoreBaseTests PRIVATE -DEXPECTED_INCLUDE_DIR="${CMAKE_BINARY_DIR}/include")
 
 ROOT_ADD_GTEST(CoreErrorTests TErrorTests.cxx LIBRARIES Core)
 
diff --git a/core/base/test/TROOTTests.cxx b/core/base/test/TROOTTests.cxx
index 5bc454b9e164a..0e3c097ef20c0 100644
--- a/core/base/test/TROOTTests.cxx
+++ b/core/base/test/TROOTTests.cxx
@@ -41,3 +41,13 @@ TEST(TROOT, GetSharedLibDir)
 
    EXPECT_EQ(libDir, libDirRef);
 }
+
+TEST(TROOT, GetIncludeDir)
+{
+   namespace fs = std::filesystem;
+
+   fs::path includeDir = gROOT->GetIncludeDir().Data();
+   fs::path includeDirRef = EXPECTED_INCLUDE_DIR;
+
+   EXPECT_EQ(includeDir, includeDirRef);
+}