Carotenoid-based polymorphisms are widespread in populations of birds, fish, and reptiles, but generally little is known about the factors affecting their maintenance in populations. We report a combined field and molecular-genetic investigation of a nestling beak color polymorphism in Darwin’s finches. Beaks are pink or yellow, and yellow is recessive. Here we show that the polymorphism arose in the Galápagos half a million years ago through a mutation associated with regulatory change in the BCO2 gene and is shared by 14 descendant species. The polymorphism is probably a balanced polymorphism, maintained by ecological selection associated with survival and diet. In cactus finches, the frequency of the yellow genotype is correlated with cactus fruit abundance and greater hatching success and may be altered by introgressive hybridization. Polymorphisms that are hidden as adults, as here, may be far more common than is currently recognized, and contribute to diversification in ways that are yet to be discovered.