Sharks are iconic predators in today's oceans, yet their modern diversity has ancient origins. In particular, present hypotheses suggest that a combination of mass extinction, global climate change, and competition has regulated the community structure of dominant mackerel (Lamniformes) and ground (Carcharhiniformes) sharks over the last 66 million years. However, while these scenarios advocate an interplay of major abiotic and biotic events, the precise drivers remain obscure. Here, we focus on the role of feeding ecology using a geometric morphometric analysis of 3,837 fossil and extant shark teeth. Our results reveal that morphological segregation rather than competition has characterized lamniform and carcharhiniform evolution. Moreover, although lamniforms suffered a long-term disparity decline potentially linked to dietary "specialization," their recent disparity rivals that of "generalist" carcharhiniforms. We further confirm that low eustatic sea levels impacted lamniform disparity across the end-Cretaceous mass extinction. Adaptations to changing prey availability and the proliferation of coral reef habitats during the Paleogene also likely facilitated carcharhiniform dispersals and cladogenesis, underpinning their current taxonomic dominance. Ultimately, we posit that trophic partitioning and resource utilization shaped past shark ecology and represent critical determinants for their future species survivorship.