Sperm guidance is controlled by chemical and physical cues. In many species, Ca²⁺ bursts in the flagellum govern navigation to the egg. In Arbacia punctulata, a model system of sperm chemotaxis, a cGMP signaling pathway controls these Ca²⁺ bursts. The underlying Ca²⁺ channel and its mechanisms of activation are unknown. Here, we identify CatSper Ca²⁺ channels in the flagellum of A. punctulata sperm. We show that CatSper mediates the chemoattractant‐evoked Ca²⁺ influx and controls chemotactic steering; a concomitant alkalization serves as a highly cooperative mechanism that enables CatSper to transduce periodic voltage changes into Ca²⁺ bursts. Our results reveal intriguing phylogenetic commonalities but also variations between marine invertebrates and mammals regarding the function and control of CatSper. The variations probably reflect functional and mechanistic adaptations that evolved during the transition from external to internal fertilization.