The production of sex pheromones can impose significant costs on the signalling sex if the precursor substances are limited. Therefore, maintaining a costly pheromone system requires an increase of mating opportunities associated with its use. For a long time, it was assumed that mating in the parasitoid Nasonia giraulti takes place prior to emergence within the host. Mated females, however, no longer respond to the male sex attractant raising the question of why males afford to produce the costly chemical signal. Here we show that males invest about a quarter of their teneral lipid reserves in pheromone production and release more than 60% of the stored pheromone after successful mating likely to attract more virgin females that are about to emerge. Most N. giraulti females emerging from hosts exclusively parasitized by this species, however, were mated and therefore unresponsive to the male pheromone. In contrast, when hosts were parasitized also by the sympatric congeneric species N. vitripennis, most N. giraulti females emerged unmated and were attracted by the pheromone of conspecific males. Multiparasitism is widespread among the two Nasonia species studied here, thus explaining the investment of fitness-relevant amounts of resources in a functional pheromone system in N. giraulti males.