The Northwestern Hawaiian Islands share comparable biological community structures and have similar histories of fishing pressure, yet monk seal subpopulations show different trends of decline between locations. Using trophic models, we compared ecosystem structure and energy flows supporting 2 subpopulations (on Laysan Island and French Frigate Shoals (FFS) atoll), each with varied rates of decline (1998−2015). Through simulated perturbations, we showed that the Laysan community had much higher productivity and was mainly forced by bottom-up processes, but prey and predator abundance also controlled the energy flow and community structure. The FFS ecosystem was less productive and strongly influenced by a change in primary productivity. Although the FFS system responded to a change in predator and prey abundance, the monk seals were more influenced by benthic bottomfish biomass than by a change in predator abundance. We clarified the role of external drivers (Pacific Decadal Oscillation [PDO] and benthic bottomfish fishery): while the PDO did show correlation with monk seal population trends, the best models were driven by prey biomass as impacted by bottomfish removals. However, monk seal predator and prey trophic dynamics were not sufficient to explain the observed decline in monk seal biomass. We suggest that other factors amplifying mortality played a role; for example, shark predation on monk seal pups at FFS. Because of the uncertainties inherent in a complex ecosystem model, the results cannot be used for tactical management but they can help direct management or future research efforts in the recovery of the endangered monk seal population.