The costs and benefits of mating are frequently measured in order to understand why females mate multiply. However, to separate the factors that initiate the evolution of polyandry (from monandry) from the factors that maintain it, we must ascertain how the environment changes the economics of mating. Here we show how context-dependent costs of mating can lead to the evolution of polyandry in a species that is monandrous in the wild, the parasitoid wasp Nasonia vitripennis. We have previously shown that when females have insufficient time between mating and ovipositing, they appear unable to process sperm effectively and end up overproducing sons (i.e. laying unfertilised eggs, since Nasonia is in haplodiploid). This overproduction of sons is costly due to selection on sex allocation in this species. Although N. vitripennis is monandrous in the wild, polyandry evolves under laboratory culture despite this sex allocation cost. In this study we show why: when groups of females oviposit together, as in laboratory culture, selection on sex allocation via Local Mate Competition (LMC) is reduced, increasing the reproductive value of sons. This relaxes the fitness cost of male production. Overproduction of sons still occurs, but it is penalised less than when females oviposit alone, under high LMC conditions, as they typically do in the field. Our results highlight how the costs and benefits of mating can vary under different ecologically relevant conditions, in this case the spatio-temporal distribution of resources and competitors, promoting the evolution of polyandry from monandry, and vice versa.