When there is conspicuous underexploitation of a limited resource, it is worth asking, what mechanisms allow presumably valuable resources to be left unused? Evolutionary biologists have generated a wide variety of hypotheses to explain this, ranging from interdemic group selection to selfishly prudent individual restraint. We consider a situation in which, despite high intraspecific competition, individuals leave most of a key resource unexploited. The parasitic wasp that does this finds virtually all host egg clusters in a landscape but parasitizes only about a third of the eggs in each and then leaves a deterrent mark around the cluster. We first test-and reject-a series of system-specific simple constraints that might limit full host exploitation, such as asynchronous maturation of host eggs. We then consider classical hypotheses for the evolution of restraint. Prudent predation and bet-hedging fail as explanations because the wasp lives as a large, well-mixed population. Additionally, we find no individual benefits to the parasitoid of developing in a sparsely parasitized host nest. However, an optimal foraging model, including empirically measured costs of superparasitism and hyperparasitism, can explain through individual selection both the consistently low rate of parasitism and deterrent marking.