Investigating the patterns of evolutionary diversification is vital to understanding the processes governing the rich biodiversity of vertebrates. Habitat can provide ecological opportunity and serve as a catalyst for evolution, resulting in the unequal spread of phenotypic disparity across ecosystems. While both marine and freshwater environments harbor significant portions of fish diversity, they offer a particularly intriguing evolutionary juxtaposition. The different biogeographic and environmental factors between the two ecosystems can have substantial effects on morphological diversification. Yet, both environments offer similar opportunities for diversification within benthic, demersal, and pelagic regimes, which lineages have radiated into with consistent phenotypic trends. Here, we investigate whether the axis of body shape diversity within each of these habitats differs between fishes in marine and freshwater systems. Using specimens from the Smithsonian Museum, we developed a dataset of linear measurements capturing body shape in 2,200 freshwater and 3,300 marine teleost species. By comparing angles between the first principal components, we find that the fish body shapes in corresponding regimes have more similar primary axes of diversity than would be expected by chance, but that different processes are driving these parallel patterns in freshwater and marine environments. Marine diversification is generally phylogenetically constrained, which may indicate widespread phylogenetic niche conservatism. In contrast, ecological signal appears to overpower phylogenetic constraints in freshwater lineages. In spite of these divergent evolutionary processes, our findings imply that habitat imposes strong selective pressures, driving consistent patterns of evolutionary diversification on a global scale.