Ants originated over 150 million years ago through an irreversible transition to superorganismal colony life. Comparative analyses of 163 ant genomes, including newly generated whole-genome sequences of 145 ant species, reveal extensive genome rearrangements correlated with speciation rates. Meanwhile, conserved syntenic blocks are enriched with co-expressed genes involved in basal metabolism and caste differentiation. Gene families related to digestion, endocrine signaling, cuticular hydrocarbon synthesis, and chemoreception expanded in the ant ancestor, while many caste-associated genes underwent positive selection in the formicoid ancestor. Elaborations and reductions of queen-worker dimorphism and other social traits left convergent signatures of intensified or relaxed selection in conserved signaling and metabolic pathways, suggesting that a core gene set was used to diversify organizational complexity. Previously uncharacterized genetic regulators of caste development were confirmed by functional experiments. This study reconstructs the genetic underpinning of social traits and their integration within gene-regulatory networks shaping caste phenotypes.