Teleost fishes make up almost half of extant vertebrate biodiversity. The evolutionary success of teleosts has been attributed to the emergence of a homocercal configuration of their caudal skeleton. Considered a synapomorphy and key innovation of teleosts, homocercality, i.e. superficial dorso-ventral (DV) symmetry, enables more sophisticated modes of swimming compared to the ancestral heterocercal condition, i.e. DV asymmetry. The genetic evolutionary mechanisms underlying the emergence of the homocercal configuration in the teleost ancestor have yet to be uncovered. We test the hypothesis that differential outgrowth of two caudal structures in fish, 1.) the ‘tail’ (the terminal notochord and associated structures) and 2.) the caudal fin ultimately resulted in the diversity of caudal morphologies in ray-finned fishes and vertebrates in general. We compare caudal development in the homocercal teleost zebrafish (Danio rerio) with the heterocercal spotted gar (Lepisosteus oculatus), representing the closest living outgroup to teleosts, through comparative genomics, morphological studies, gene expression analyses, and chromatin profiling, we identify candidate genes and regulatory elements for caudal region development and evolution among ray-finned fishes.