Given the costs of multiple-mating, why has female polyandry evolved? Utetheisa ornatrix moths are well-suited for studying multiple mating in females because females are highly polyandrous over their lifespan, with each male mate transferring a substantial spermatophore with both genetic and non-genetic material. The accumulation of resources might explain the prevalence of polyandry in this species, but another, not mutually-exclusive, possibility is that females mate multiply to increase the probability that their sons will inherit more-competitive sperm. This latter “sexy-sperm” hypothesis posits that female multiple mating and male sperm competitiveness co-evolve via a Fisherian runaway process. We tested the sexy-sperm hypothesis by using competitive double matings to compare the sperm competition success of sons of polyandrous versus monandrous females. In accordance with sexy-sperm theory, we found that in 511 offspring across 17 families, the male whose polyandrous mother mated once with each of three different males sired significantly more of all total offspring (81%) than did the male whose monandrous mother was mated thrice to a single male. Interestingly, sons of polyandrous mothers had a significantly biased sex ratio of their brood toward sons, also in support of the hypothesis.