The evolution of eusociality is a perennial issue in evolutionary biology, and genomic advances have fueled steadily growing interest in the genetic changes underlying social evolution. Along with a recent flurry of research on comparative and evolutionary genomics in different eusocial insect groups (bees, ants, wasps, and termites), several mechanistic explanations have emerged to describe the molecular evolution of eusociality from solitary behavior. These include solitary physiological ground plans, genetic toolkits of deeply conserved genes, evolutionary changes in protein-coding genes, cis regulation, and the structure of gene networks, epigenetics, and novel genes. Despite this proliferation of ideas, there has been little synthesis, even though these ideas are not mutually exclusive and may in fact be complementary. We review available data on molecular evolution of insect sociality and highlight key biotic and abiotic factors influencing social insect genomes. We then suggest both phylogenetic and ecological evolutionary developmental biology (eco-evo-devo) perspectives for a more synthetic view of molecular evolution in insect societies.