The influence of depth and associated gradients in light, nutrients and plankton on the ecological organization of tropical reef communities was first described over six decades ago but remains untested across broad geographies. During this time humans have become the dominant driver of planetary change, requiring that we revisit historic ecological paradigms to ensure they capture the dynamics of contemporary ecological systems. Analysing >5,500 in-water reef fish surveys between 0 and 30 m depth on reef slopes of 35 islands across the Pacific, we assess whether a depth gradient consistently predicts variation in reef fish biomass. We reveal predictable ecological organization at unpopulated locations, with increased biomass of planktivores and piscivores and decreased primary consumer biomass with increasing depth. Bathymetric steepness also had a striking influence on biomass patterns, primarily for planktivores, emphasizing potential links between local hydrodynamics and the upslope propagation of pelagic subsidies to the shallows. However, signals of resource-driven change in fish biomass with depth were altered or lost for populated islands, probably due to depleted fish biomass baselines. While principles of depth zonation broadly held, our findings expose limitations of the paradigm for predicting ecological dynamics where human impacts confound connections between ecological communities and their surrounding environment.