With the exception of the final stages of spermatogenesis in butterfly and some unicellular ciliates and flagellates, ciliated cells undergo cell division without cilia. This reciprocal relationship between cilia formation and cell division has prompted investigators to propose that ciliogenesis and cell cycle progression are mutually exclusive processes. Early work in fibroblasts showed that deciliation occurs in two waves, as cells depart from quiescence. The first wave of deciliation occurs before entry into S, while the second wave occurs between S and mitosis. Since then, it has remained a mystery whether and how (de)ciliation is coupled to the cell cycle and further, whether ciliation can affect cell cycle progression. Several recent publications provide evidence for a causative role of ciliary resorption in influencing the duration of the G1 phase of the cell cycle impacting on several developmental processes, including left-right patterning, kidney, skeletal and brain development. This body of work argues for the existence of a molecular crosstalk between ciliary factors and regulators of the cell cycle. Here, we review the evidence connecting primary cilia and the cell cycle and evaluate the idea that the primary cilium may function as a physical checkpoint in cell cycle re-entry.