The primary cilium, critical for morphogenic and growth factor signaling, is assembled upon cell cycle exit, but the links between ciliogenesis and cell cycle progression are unclear. K V10.1 is a voltage‐gated potassium channel frequently overexpressed in tumors. We have previously reported that expression of K V10.1 is temporally restricted to a time period immediately prior to mitosis in healthy cells. Here, we provide microscopical and biochemical evidence that K V10.1 localizes to the centrosome and the primary cilium and promotes ciliary disassembly. Interference with K V10.1 ciliary localization abolishes not only the effects on ciliary disassembly, but also K V10.1‐induced tumor progression in vivo. Conversely, upon knockdown of K V10.1, ciliary disassembly is impaired, proliferation is delayed, and proliferating cells show prominent primary cilia. Thus, modulation of ciliogenesis by K V10.1 can explain the influence of K V10.1 expression on the proliferation of normal cells and is likely to be a major mechanism underlying its tumorigenic effects.