The Siluro-Devonian adaptive radiation of jawed vertebrates, which underpins almost all living vertebrate biodiversity, is characterised by the evolutionary innovation of the lower jaw. Multiple lines of evidence have suggested that the jaw evolved from a rostral gill arch, but when the jaw took on a feeding function remains unclear. We quantified the variety of form in the earliest jaws in the fossil record and , from which we generated a range of theoretical morphospacelogies within this morphological range, which that we then tested for their functional optimality. By drawing comparisons with the real jaw data and reconstructed ancestral forms, our results show that the earliest jaw shapes were optimised for fast closure and stress resistance, inferring a feeding rather than solely ventilation function. Jaw shapes then became less optimal for these functions during the later radiation of jawed vertebrates. Thus, the evolution of jaw morphology has continually explored new morphospace and accumulated disparity through time, laying the foundation for diverse feeding strategies and the success of jawed vertebrates.