Supergenes, or regions of the genome containing two or more linked functional mutations that control complex traits, are emerging as a common genetic basis for many striking phenotypic polymorphisms in insects. Now that we know that supergenes are common, we can seek common features of diverse supergene systems. Here, we lay out a framework of open questions (see graphical abstract) that can be addressed separately in each system and, ultimately, compared across systems to seek general patterns in supergene evolution. Few empirical studies have investigated what causes new supergene haplotypes to initially increase in frequency, but to not eventually fix in a population. Resolving the genotype-phenotype connection and isolating functional genes will provide more insight into the forms of selecting shaping supergene evolution. Ultimately, research on supergenes will help to broaden our understanding of how recombination rate variation influences the evolutionary trajectories of sexually reproducing organisms.