Mammalian centrioles fulfill a number of important roles throughout the cell cycle, establishing a microtubule organizing center (MTOC) in interphase and ensuring high fidelity chromosome separation in mitosis. Additionally, they have the capacity to act as basal bodies that nucleate the assembly of cilia. While controls must be present to regulate these different fates, key components remain largely undefined. We have employed a biochemical approach to purify complexes associated with CP110, a protein which has been previously shown to have an essential role in centrosome duplication and cytokinesis, and have identified two novel centriolar proteins, Cep97 and Cep76. Knockdown of Cep97 by RNAi or expression of dominant-negative mutants leads to CP110 displacement from centrosomes, mitotic spindle defects, and cytokinesis failure. Strikingly, loss of either Cep97 or CP110 results in an induction of primary cilia formation in cycling cells, suggesting that Cep97 and CP110 work together to inhibit a ciliogenesis program during the times when free centrioles are needed to assure chromosome segregation. Cilia formation may be a default pathway engaged in the absence of CP110 function, since enforced expression of CP110 in quiescent cells suppresses the ability to assemble cilia. Cep76 interacts with the CP110-Cep97 complex at the centrosome and appears to play a role in limiting centriole duplication to once per cell cycle, as evident from the presence of supernumerary centrioles in cells depleted of Cep76. Detailed characterization of Cep97, Cep76 and other genes involved in key centriolar processes throughout the cell cycle will enrich our understanding of human diseases associated with centrosomal and ciliary defects, enabling novel therapeutic strategies.