Malaria, which is caused by Plasmodium parasites, is transmitted by anopheline mosquitoes. When gametocytes, the precursor cells of Plasmodium gametes, are transferred to a mosquito, they fertilize and proliferate, which render the mosquito infectious to the next vertebrate host. Although the fertilization of malaria parasites has been considered as a rational target for transmission-blocking vaccines, the underlying mechanism is poorly understood. Here, we show that the rodent malaria parasite gene Plasmodium berghei GENERATIVE CELL SPECIFIC 1 (PbGCS1) plays a central role in its gametic interaction. PbGCS1 knockout parasites show male sterility, resulting in unsuccessful fertilization. Because such a male-specific function of GCS1 has been observed in angiosperms, this indicates, for the first time, that parasite sexual reproduction is controlled by a machinery common to flowering plants. Our present findings provide a new viewpoint for understanding the parasitic fertilization system and important clues for novel strategies to attack life-threatening parasites.