Male reproductive success in the lesser wax moth Achroia grisella is strongly determined by pre-copulatory mate choice, during which females choose among males aggregated in small leks based on the attractiveness of ultrasonic songs. Nothing is known about the potential of post-copulatory mechanisms to affect male reproductive success. However, there is evidence that females at least occasionally remate with a second male and that males are unable to produce ejaculates quickly after a previous copulation. Here we investigated the effects of mating history on ejaculate size and demonstrate that the number of transferred sperm significantly decreased from first (i.e., virgin) to second (i.e., nonvirgin) copulation within individual males. For males of identical age, the number of sperm transferred was higher in virgin than in nonvirgin copulations, too, demonstrating that mating history, is responsible for the decrease in sperm numbers transferred and not the concomitant age difference. Furthermore, the number of transferred sperm was significantly repeatable within males. The demonstrated variation in ejaculate size both between subsequent copulations as well as among individuals suggests that there is allocation of a possibly limited amount of sperm. Because female fecundity is not limited by sperm availability in this system, post-copulatory mechanisms, in particular sperm competition, may play a previously underappreciated role in the lesser wax moth mating system.