How do developmental mechanisms evolve to control changing skeletal morphology, the shapes and sizes of individual bones? We address this question with studies of the opercle (OP), a large facial bone that has undergone marked morphological evolution in the ray-finned fish. Attributes for developmental analysis motivated us to examine how OP shape and size evolve and develop in threespine sticklebacks, a model system for understanding vertebrate evolution. We find that when Alaskan anadromous fish take up permanent residence in lakes, they evolve smaller and reshaped OPs. The change is a reduction in the amount of bone laid down along one body axis, and it arises at or shortly after the onset of OP development. A quantitative trait locus is present on linkage group 19 that contributes in a major way to this phenotype.