Tropical marine ecosystems are under mounting anthropogenic pressure from overfishing and habitat destruction, leading to declines in their structure and function on a global scale. Although maintaining connectivity among habitats within a seascape is necessary for preserving population resistance and resilience, quantifying movements of individuals within seascapes remains challenging. Traditional methods of identifying and valuing potential coral reef fish nursery habitats are indirect, often relying on visual surveys of abundance and correlations of size and biomass among habitats. We used compound-specific stable isotope analyses to determine movement patterns of commercially important fish populations within a coral reef seascape. This approach allowed us to quantify the relative contributions of individuals from inshore nurseries to reef populations and identify migration corridors among important habitats. Our results provided direct measurements of remarkable migrations by juvenile snapper of over 30 km, between nurseries and reefs. We also found significant plasticity in juvenile nursery residency. Although a majority of individuals on coastal reefs had used seagrass nurseries as juveniles, many adults on oceanic reefs had settled directly into reef habitats. Moreover, seascape configuration played a critical but heretofore unrecognized role in determining connectivity among habitats. Finally, our approach provides key quantitative data necessary to estimate the value of distinctive habitats to ecosystem services provided by seascapes.