Recent progress has been made in identifying genomic regions implicated in trait evolution on a microevolutionary scale in many species, but whether these are relevant over macroevolutionary time remains unclear. Here, we directly address this fundamental question using bird beak shape, a key evolutionary innovation linked to patterns of resource use, divergence and speciation, as a model trait. We design a novel approach by integrating class-wide geometric-morphometric analyses with evolutionary sequence analyses of 10,322 protein coding genes as well as 229,001 genomic regions spanning 72 species. We identify 1,434 protein coding genes and 39,806 non-coding regions for which molecular rates were significantly related to rates of bill shape evolution. We show that homologs of the identified protein coding genes as well as genes in close proximity to the identified non-coding regions are involved in craniofacial embryo development in mammals. We identify two associated pathways, BMP and Wnt signalling, both of which have repeatedly been implicated in the morphological development of avian beaks. This result suggests that our approach identifying genotype-phenotype association on a genome wide scale over macroevolutionary time is feasible. While the coding and non-coding gene sets are associated with similar pathways, the actual genes are highly distinct, with significantly reduced overlap between them and bill-related phenotype associations specific to non-coding loci. Moreover we find evidence for signatures of recent diversifying selection in the identified non-coding loci in populations of Darwin’s finches that differ notably in their beak shape morphology. Our results suggest that regulatory rather than coding changes are major drivers of morphological diversification over macroevolutionary times.