Changes in the physical environment are major drivers of evolutionary change, either through direct effects on the distribution and abundance of species or more subtle shifts in the outcome of biological interactions. To investigate this phenomenon, we built a fossil data set of drilling gastropod predation on bivalve prey for the last 11 Myr to determine how the regional collapse in Caribbean upwelling and planktonic productivity affected predator–prey interactions. Contrary to theoretical expectations, predation increased nearly twofold after productivity declined, while the ratio of drilling predators to prey remained unchanged. This increase reflects a gradual, several-fold increase in the extent of shallow-water coral reefs and seagrass meadows in response to the drop in productivity that extended over several million years. Drilling predation is uniformly higher in biogenic habitats than in soft sediments. Thus, changes in predation intensity were driven by a shift in dominant habitats rather than a direct effect of decreased productivity. Most previous analyses of predation through time have not accounted for variations in environmental conditions, raising questions about the patterns observed. More fundamentally, however, the consequences of large-scale environmental perturbations may not be instantaneous, especially when changes in habitat and other aspects of local environmental conditions cause cascading series of effects.