When there is conspicuous under-exploitation of a limited resource it is worth asking, what mechanism makes it beneficial to leave presumably valuable resources unused? Evolutionary biologists have generated a wide range of hypotheses to explain this, ranging from interdemic group selection to selfishly prudent individual restraint. We consider a situation in which, in spite of 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 parasitize only about a third of the eggs in each. 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. Also, we find no individual benefits to the parasitoid of developing in a sparsely parasitized host nest. However an optimal foraging model, including empirically measured cost of superparasitism and risk of hyperparasitism, can explain through individual selection, both the consistently low rate of parasitism and marking.