Paleozoic sphenacodontid synapsids are the oldest known fully terrestrial apex predators. Dimetrodon and other sphenacodontids are the first terrestrial vertebrates to have strong heterodonty, massive skulls and well-developed labio-lingually compressed and recurved teeth with mesial and distal cutting edges (carinae). Here we reveal that the dentition of Dimetrodon and other sphenacodontids is diverse. Tooth morphology includes simple carinae with smooth cutting edges and elaborate enamel features, including the first occurrence of cusps and true denticles (ziphodonty) in the fossil record. A time-calibrated phylogenetic analysis indicates that changes in dental morphology occur in the absence of any significant changes in skull morphology, suggesting that the morphological change is associated with changes in feeding style and trophic interactions in these ecosystems. In addition, the available evidence indicates that ziphodonty evolved for the first time in the largest known species of the genus Dimetrodon and independently from the ziphodont teeth observed in some therapsids.