How are skilled motor behaviors – such as the ability to sing and dance – encoded genetically? A diverse array of circuits and cell types all work in concert to produce behavior, the result of millions of years of evolutionary optimization at the level of the genome. Genetic changes resulting in the evolution of novel behaviors are rarely identified in genes themselves, which are highly conserved across species. Rather, recent work suggests a critical role for the other 98% of the genome, the noncoding regions that orchestrate gene activity. To elucidate the relationship between motor behavior and sequence evolution, we sequenced and extensively analyzed the genomes of 5 manakins (Pipridae), an avian family characterized by their extreme sexual dimorphism. Males of various species engage in virtuosic courtship dances, involving leaps, loops, and moonwalks that are as rapid as they are precise. We identified manakin gene regulatory specializations through a comparison of thousands of conserved noncoding elements (CNEs) across dozens of additional avian genomes. A subset of these CNEs was found to be evolutionarily accelerated uniquely in the manakin lineage. These elements are not randomly distributed across the genome, but rather are clustered around genes relevant to manakin behavior, including steroid signaling, motor learning, and brain development. We localized the expression of a subset of these genes to brain areas involved in fast visual tracking, suggesting that the CNEs proximal to these genes may represent regulatory regions associated with the perception of manakins’ high-speed courtship displays. In sum, this work provides a template for how we might accelerate discovery into the regulatory genomic mechanisms of behavior through a neuroethological approach to comparative genomics.