Organisms have utilized group living as a strategy for enhancing their survival and reproduction for millennia. A notable species displaying the most advanced group living, termed eusociality, is the fire ant Solenopsis invicta. This species is socially polymorphic, having two social forms genetically determined by a large supergene. Our goal is to explore the evolutionary implications of S. invicta colonies having multiple egg-laying queens (polygyny). We show that: 1) reproductive skew, or unequal sharing of maternity among nestmate queens, invariably occurs when there is more than one reproductive queen contributing to offspring production; 2) skew is significantly more pronounced among daughters of the sexual caste than daughters of the sterile worker caste; and 3) overrepresentation of the Sb supergene occurs in the sexual daughter caste, but not the worker caste. This study illuminates important elements of queen reproductive strategies and colony genetic structure in polygyne S. invicta.