Centriole biogenesis and maintenance are crucial for cells to generate cilia and assemble centrosomes that function as microtubule organizing centers (MTOCs). Centriole biogenesis and MTOC function both require the microtubule nucleator -tubulin ring complex (TuRC). It is widely accepted that TuRC nucleates microtubules from the pericentriolar material (PCM) that is associated with the proximal part of centrioles. However, TuRC also localizes more distally and in the centriole lumen, but the significance of these findings is unclear. Here we identify spatially and functionally distinct sub-populations of centrosomal TuRC. Luminal localization is mediated by augmin, which is linked to the centriole inner scaffold through POC5. Disruption of luminal localization impairs centriole integrity and interferes with cilium assembly. Defective ciliogenesis is also observed in TuRC mutant fibroblasts from a patient suffering from microcephaly with chorioretinopathy. These results identify a novel, non-canonical role of augmin-γTuRC in the centriole lumen that is linked to human disease.