It has long been of interest to identify the phenotypic traits that mediate reproductive isolation between related species, and more recently, the genes that underpin them. Much work has focused on identifying genes associated with animal colour, with the candidate gene CYP2J19 identified in laboratory studies as the ketolase converting yellow dietary carotenoids to red ketocarotenoids in birds with red pigments. But evidence that CYP2J19 explains variation between red and yellow feather coloration in wild populations of birds is lacking. Hybrid zones between related species provide the opportunity to identify genes associated with specific traits. Here we investigate genomic regions associated with forecrown colour in red-fronted and yellow-fronted tinkerbirds across a hybrid zone in southern Africa. We sampled 79 individuals, measuring spectral reflectance of forecrown feathers as well as scoring colours from photographs. We performed a genome-wide association study to identify associations with carotenoid-based coloration, using double-digest RAD sequencing aligned to a short-read whole genome of a Pogoniulus tinkerbird that we assembled. Admixture mapping using 104,933 SNPs identified a region of chromosome 8 that includes CYP2J19 as the only locus with more than two SNPs significantly associated with both crown hue and crown score. The hybrid zone was bimodal with asymmetric backcrossing, consistent with the hypothesis that yellow-fronted females mate more often with red-fronted males than vice versa. Female red-fronted tinkerbirds mating assortatively with red-crowned males may reinforce species divergence and is consistent with the hypothesis that converted carotenoids are an honest signal of quality.