Populations experiencing consistent differences in predation risk and resource availability are expected to follow divergent evolutionary trajectories. For example, live-history theory makes specific predictions for how predation should drive life-history evolution, and according to the Trexler-DeAngelis model for the evolution of matrotrophy, post-fertilization maternal provisioning is most likely to evolve in environments with consistent, high levels of resource availability. Using the model system of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes with and without the piscivorous bigmouth sleeper (Gobiomorus dormitor), we provide some of the strongest tests of these predictions to date, as resource availability does not co-vary with predation regime in this system, and we examine numerous (14) isolated natural populations. We found clear evidence for the expected life-history divergence between predation regimes, and empirical support of the Trexler-DeAngelis model. Moreover, based on molecular and lab-rearing data, our study offers strong evidence for convergent evolution of similar life histories in similar predation regimes, largely matching previous phenotypic patterns observed in other poeciliid lineages (Brachyrhaphis spp., Poecilia reticulata), and further supports the notion that matrotrophy is most likely to evolve in stable high-resource environments.