Significance Body shape is a strong predictor of habitat occupation in fishes, which changes rapidly at microevolutionary scales in well-studied freshwater systems such as sticklebacks and cichlids. Deep-bodied forms tend to occur in benthic habitats, while pelagic species typically have streamlined body plans. The recurrent evolution of this pattern across distantly related groups suggests that limited sets of high-fitness solutions exist due to environmental constraints. We rigorously test these observations showing that similar constraints operate at deeper evolutionary scales in a clade (Lutjanidae) of primarily benthic fish dwellers that repeatedly transitioned into midwater habitats in all major oceans throughout its 45-million-year history. Midwater species strongly converge in body shape, emphasizing evolutionary determinism in form and function along the benthic–pelagic axis.