A central challenge for predators is achieving positive energy balance when prey are spatially and temporally heterogeneous. Ecological heterogeneity produces evolutionary trade-offs in the physiological design of predators; this is because the ability to capitalize on pulses of food abundance requires high capacity for food-processing, yet maintaining such capacity imposes energetic costs that are taxing during periods of food scarcity1, 2. Recent advances in physiology show that when variation in foraging opportunities is predictable, animals may adjust energetic trade-offs by rapidly modulating their digestive system to track variation in foraging opportunities1. However, it is increasingly recognized that foraging opportunities for animals are unpredictable3, which should favour animals that maintain a capacity for food-processing that exceeds average levels of consumption (loads)2, 4. Despite this basic principle of quantitative evolutionary design, estimates of digestive load:capacity ratios in wild animals are virtually non-existent1. Here we provide an extensive assessment of load:capacity ratios for the digestive systems of predators in the wild, compiling 639 estimates across 38 species of fish. We found that piscine predators typically maintain the physiological capacity to feed at daily rates 2–3 times higher than what they experience on average. A numerical simulation of the trade-off between food-processing capacity and metabolic cost suggests that the observed level of physiological opportunism is profitable only if predator–prey encounters, and thus predator energy budgets, are far more variable in nature than currently assumed.