Theory suggests evolutionary change can significantly influence and act in tandem with ecological forces via ecological-evolutionary feedbacks. This theory assumes that significant evolutionary change occurs over ecologically relevant timescales and that phenotypes have differential effects on the environment. Here we test the hypothesis that local adaptation causes ecosystem structure and function to diverge. We demonstrate that populations of Trinidadian guppies (Poecilia reticulata), characterized by differences in phenotypic and population-level traits, differ in their impact on ecosystem properties. We report results from a replicated, common garden mesocosm experiment and show that differences between guppy phenotypes result in the divergence of ecosystem structure (algal, invertebrate, and detrital standing stocks) and function (gross primary productivity, leaf decomposition rates, and nutrient flux). These phenotypic effects are further modified by effects of guppy density. We evaluated the generality of these effects by replicating the experiment using guppies derived from two independent origins of the phenotype. Finally, we tested the ability of multiple guppy traits to explain observed differences in the mesocosms. Our findings demonstrate that evolution can significantly affect both ecosystem structure and function. The ecosystem differences reported here are consistent with patterns observed across natural streams and argue that guppies play a significant role in shaping these ecosystems.