In the face of rapid anthropogenic environmental change, it is increasingly important to understand how ecological and evolutionary interactions affect the persistence of natural populations. Augmented gene flow has emerged as a potentially effective management strategy to counteract negative consequences of genetic drift and inbreeding depression in small and isolated populations. However, questions remain about the long-term impacts of augmented gene flow and whether changes in individual and population fitness are reflected in ecosystem structure, potentiating eco-evolutionary feedbacks. In this study, we used Trinidadian guppies (Poecilia reticulata) in experimental outdoor mesocosms to assess how populations with different recent evolutionary histories responded to a scenario of severe population size reduction followed by expansion in a high-quality environment. We also investigated how variation in evolutionary history of the focal species affected ecosystem dynamics. We found that evolutionary history (i.e., gene flow versus no gene flow) consistently predicted variation in individual growth. In addition, gene flow led to faster population growth in populations from one of the two drainages, but did not have measurable impacts on the ecosystem variables we measured: zooplankton density, algal growth, and decomposition rates. Our results suggest that benefits of gene flow may be long-term and environment-dependent. Although small in replication and duration, our study highlights the importance of eco-evolutionary interactions in determining population persistence and sets the stage for future work in this area.