The widespread phenomenon of polyandry (mating by females with multiple males) is an evolutionary puzzle, because females can sustain costs from promiscuity, whereas full fertility can be provided by a single male. Using the red flour beetle, Tribolium castaneum, we identify major fitness benefits of polyandry to females under inbreeding, when the risks of fertilization by incompatible male haplotypes are especially high. Fifteen generations after inbred populations had passed through genetic bottlenecks, we recorded increased levels of female promiscuity compared with noninbred controls, most likely due to selection from prospective fitness gains through polyandry. These data illustrate how this common mating pattern can evolve if population genetic bottlenecks increase the risks of fitness depression due to fertilization by sperm carrying genetically incompatible haplotypes.