In this work, I investigate the biomechanics of a 295-million-year-old proto-mammal, Dimetrodon, using a series of models and experiments to recreate their jaw as accurately as possible. Using a combination of 2D images and computed tomography scans, virtual fossils were created in 3D. This project is the first use of finite element analysis and multibody dynamics analysis in the genus. For the first time, dental microanatomy including denticles and plicidentine was modelled in 3D with individual material properties. Three separate muscle topologies of Dimetrodon were sculpted for the first time in 3D to determine individual muscle performance and a maximum combined effective bite adduction force of 4000N. Different tooth morphologies influenced the biomechanical performance of Dimetrodon’s bite. Both the incisiform and caniniform teeth were able to function effectively at maximum bite force; however, the post-caniniform teeth were unable to dissipate stress at these levels. Enamel denticles created complex patterns of localized stress across the enamel-dentine junction into the core of the crown. Elongation of the tooth roots increased the ability of the alveolar bone to cushion kinetic energy before being transmitted to the surrounding jawbone. Examining the stress and strain distribution patterns through the skull of Dimetrodon necessitated revisiting proposed topologies of the animal’s adductor musculature. The most recent reconstruction, the reptilian style of muscle attachment, is the most efficient arrangement of the muscles. The rhynchocephalian style had the highest muscle volume and produced a larger bite force estimate from the dry skull method. Predictive models based on physiological cross-sectional muscle areas are cautioned against. This model returned a bite force similar to extant hypercarnivores, and combined with little fossil evidence of bone comminution, suggests Dimetrodon was not limited by prey size and could consume the flesh of large-bodied animals.