In vertebrates, a functional jaw apparatus requires a hinge joint, so jaw joint defects are often highly disruptive. To describe the consequences of jaw-joint dysfunction, we engineered two independent null alleles of a single jaw-joint marker gene, nkx3.2, in zebrafish. These mutations caused zebrafish to become functionally jawless via fusion of the upper and lower jaw cartilages. Despite their jaws being locked, nkx3.2 mutants accommodated this defect by: a) having a remodelled skull with a fixed open gape, reduced snout, and enlarged branchial region; and b) performing ram feeding in the absence of jaw-generated suction. The late onset and broad extent of phenotypic changes in the mutants suggest that modifications to the skull are induced by functional agnathia, secondarily to nkx3.2 loss-of-function. Interestingly, nkx3.2 mutants superficially resemble ancient jawless vertebrates (anaspids and thelodonts) in overall head shapes. Because no homology exists in skull elements between these taxa, the adult nkx3.2 phenotype is not a reversal, but convergence due to similar functional requirements of feeding without moveable jaws. This remarkable analogy makes the mutants a unique model with which to: a) investigate adaptive responses to perturbation in skeletal development; b) re-evaluate evolutionarily inspired interpretations of phenocopies generated by gene knockdowns and knockouts; and c) gain insights into feeding mechanics of the extinct agnathans.