Phenotypic plasticity in response to environmental cues can create distinct morphological types within populations. This variation in form, and potentially function, may be a factor in initiating population divergence and the formation of new species. Here we show the translation of sympatric, habitat-specific morphological divergence into performance differences in energy economy, maneuverability and steady-state locomotion. Littoral and pelagic bluegill sunfish ecomorphs show differences in performance that appear adaptive within their respective habitats: greater maneuverability in the heavily vegetated littoral; greater steady-state swimming speed and economy in the open-water pelagic. This represents a trade-off in unsteady versus steady swimming performance, likely because morphological features associated with maximizing maneuverability are incompatible with enhancing steady-swimming performance. This may constrain the direction of adaptive change, maintaining the divergence created by phenotypic plasticity. The combination of habitat specific sympatric adaptation and constraints imposed by performance trade-offs may be an important factor underlying the high rate of speciation in freshwater fishes from post-glacial lakes.