Progress towards understanding adaptive radiations at the mechanistic level is still limited with regard to the proximate molecular factors that both promote and constrain evolution. Here we focus on the craniofacial skeleton and show that expanded Wnt/β-catenin signalling early in ontogeny is associated with the evolution of phenotypic novelty and ecological opportunity in Lake Malawi cichlids. We demonstrate that the mode of action of this molecular change is to effectively lock into place an early larval phenotype, likely through accelerated rates of bone deposition. However, we demonstrate further that this change toward phenotypic novelty may in turn constrain evolutionary potential through the corresponding reduction in craniofacial plasticity at later stages of ontogeny. In all, our data implicate the Wnt pathway as an important mediator of craniofacial form and offer new insights into how developmental systems can evolve to both promote and constrain evolutionary change.