As preferred prey become scarce, theory suggests that predator per-capita consumption rates decline and predator diets diversify. As a keystone predator, sea otters (Enhydra lutris) are known to have remarkable impacts on their macroinvertebrate prey, however, variation in the magnitude of these effects through time remain less well known. Using a space-for-time substitution, we quantified sea otter foraging behaviour at 5 rocky reef sites that fell along a gradient in otter occupation time (0.1-33 years) on British Columbia, Canada's central coast. As site occupation time increased, sea otters targeted increasingly smaller, more diverse macroinvertebrate prey suggesting the serial depletion of preferred to less valuable prey. We found strong evidence that urchin density and occupation time were important drivers of sea otter per-capita consumption rates on urchins, strongly interacting rocky reef herbivores, well known to drive the distribution and abundance of kelps. In addition, there was greater strength of evidence for prey-dependent over predator-dependent functional response models of sea otter consumption of urchins. These results have implications for nearshore productivity, commercial and subsistence shellfish fisheries and balancing the trade-offs inherent to ecosystem-based management.