Biologists now recognize that ecology can drive evolution, and that evolution in turn produces ecological patterns. I extend this thinking to include longer time-scales, suggesting that macroevolutionary transitions can create phenotypic differences among species, which then have predictable impacts on species interactions, community assembly, and ecosystem functioning. Repeated speciation can exacerbate these patterns by creating communities with similar phenotypes and hence ecological impacts. Here, I use several experiments to test these ideas in dragonfly larvae that occupy ponds with fish, ponds without fish, or both. I show that macroevolutionary transitions between habitats cause fishless pond species to be more active relative to fish pond specialists, reducing prey abundance, shifting prey community composition, and creating stronger trophic cascades. These effects scale-up to the community level with predictable consequences for ecosystem multi-functioning. I suggest that macroevolutionary history can have predictable impacts on phenotypic traits, with consequences for interacting species and ecosystems.