While retaining ancestral morphological and genomic traits, skates evolved a novel body plan with remarkably enlarged wing-like fins that allowed skates to thrive in benthic environments, but their molecular underpinnings remain elusive. Here we investigate the origin of this phenotypical innovation by assembling a high-quality chromosome-scale genome sequence for the little skate Leucoraja erinacea and by generating extensive regulatory profiling datasets in developing fins (gene expression, chromatin occupancy and conformation). We show that despite their derived morphology, the skate genome retains multiple features of the ancestral jawed vertebrate genome. Overall design: HiC experiments in skate fins samples