While eusociality arose in species with single-mating females, multiple mating by queens has evolved repeatedly across the social ants, bees, and wasps. Understanding the benefits and costs of multiple mating of queens is important because polyandry results in reduced relatedness between siblings, reducing kin-selected benefits of helping while also selecting for secondary social traits that reduce intracolony conflict. The leading hypothesis for the benefits of polyandry in social insects emphasizes advantages of a genetically diverse workforce. Workerless social parasite species (inquilines) provide a unique opportunity to test this hypothesis, since they are derived from social ancestors but do not produce workers of their own. Such parasites are thus predicted to evolve single mating because they would experience the costs of multiple mating but not the benefits if such benefits accrue through the production of a genetically diverse group of workers. Here we show that the workerless social parasite Dolichovespula arctica, a derived parasite of wasps, has reverted to obligate single mating from a facultatively polyandrous ancestor, mirroring a similar reversion from obligate polyandry to approximate monandry in a social parasite of fungus-farming ants. This finding and a comparison with two other cases where inquilinism did not induce reversal to monandry support the hypothesis that facultative polyandry can be costly and may be maintained by benefits of a genetically diverse workforce.