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Toothed whales (odontocetes) emit high-frequency underwater sounds (echolocate)—an extreme and unique innovation allowing them to sense their prey and environment. Their highly specialized mandible (lower jaw) allows high-frequency sounds to be transmitted back to the inner ear. Echolocation is evident in the earliest toothed whales, but little research has focused on the evolution of mandibular form regarding this unique adaptation. Here, we use a high-density, three-dimensional geometric morphometric analysis of 100 living and extinct cetacean species spanning their ∼50-million-year evolutionary history. Our analyses demonstrate that most shape variation is found in the relative length of the jaw and the mandibular symphysis. The greatest morphological diversity was obtained during two periods of rapid evolution: the initial evolution of archaeocetes (stem whales) in the early to mid-Eocene as they adapted to an aquatic lifestyle, representing one of the most extreme adaptive transitions known, and later on in the mid-Oligocene odontocetes as they became increasingly specialized for a range of diets facilitated by increasingly refined echolocation. Low disparity in the posterior mandible suggests the shape of the acoustic window, which receives sound, has remained conservative since the advent of directional hearing in the aquatic archaeocetes, even as the earliest odontocetes began to receive sounds from echolocation. Diet, echolocation, feeding method, and dentition type strongly influence mandible shape. Unlike in the toothed whale cranium, we found no significant asymmetry in the mandible. We suggest that a combination of refined echolocation and associated dietary specializations have driven morphology and disparity in the toothed whale mandible. • Toothed whale jaw diversity was obtained during two key periods of rapid evolution • High evolutionary rates are seen in the increasingly aquatic archaeocetes • Highest evolutionary rates occur as the odontocetes diverge and specialize • Diet and echolocation have the strongest influence on mandible morphology Coombs et al. quantify morphology, disparity, and evolutionary rates in toothed whale mandibles. The greatest morphological diversity was obtained during the initial evolution of stem whales and later on in the mid-Oligocene odontocetes. Refined echolocation and associated dietary specializations have driven morphology in the toothed whale mandible. [ABSTRACT FROM AUTHOR]