Centrioles are evolutionary conserved, supramolecular organelles, characterized by a blade-like assembly of nine microtubule triplets. They are critical for essential cellular functions of centrosome assembly and cilium templating. Polarized with distinct microtubule-binding structures along the proximal-distal axis, the proximal region mediates centriole assembly. Seminal studies of centriole architecture in species such as Trichonympha and Chlamydomonas have provided insights into the structural organization of the proximal region, but the question remains: is this organization ubiquitous through evolution? Using cryo-electron tomography to visualize the native proximal architecture of Naegleria gruberi, Chlamydomonas reinhardii, Paramecium tetraurelia, and human centrioles, we unveiled that the cartwheel structure is a stack of ring pairs with a 4 nm periodicity, the cartwheel inner density is a conserved structural entity, and that the cartwheel is connected to the A-C linker through the triplet base, rooted in the pinhead. This work provides unprecedented insights into centriole biogenesis. Furthermore, the tomograms generated in these 4 species allowed us to explore other centriolar regions. We identified that at the centriolar core region, a helical inner scaffold interconnects the microtubule triplets, and helps to main centriole cohesion and integrity. This work has unveiled sub-structural connections previously undescribed and defined the boundaries of the proximal and central core regions. Our work has generated the most structurally comprehensive model of the centriole to date.