We suggest that supergenes, groups of co-inherited loci, may be involved in a range of intriguing genetic and evolutionary phenomena in insect societies, and may play broad roles in the evolution of cooperation and conflict. Supergenes are central in the evolution of an array of traits including self-incompatibility, mimicry, and sex chromosomes. Recently, researchers identified a large supergene, described as a social chromosome, which controls social organization in the fire ant. This system was previously considered to be a remarkable example of a single gene affecting a complex social trait. We describe how selection may commonly favor reduced recombination and the formation of supergenes for social traits, and once formed, supergenes may strongly influence further evolutionary dynamics within and between lineages. The evolution of supergenes, and even wholly non-recombining genomes, may be particularly common in systems in which genetically distinct lineages can form mutually reinforcing socially parasitic relationships.