Understanding how energy is transferred within and across ecosystems is essential to better understand drivers and future consequences of shifts in energy pathways. We used stable isotope ratios of 1932 fish individuals belonging to the 11 most abundant fish species collected across 300,000 km2 along the English Channel–Celtic Sea continuum. To examine cross‐ecosystem differences in trophic functioning, we assessed the effects of both extrinsic (depth) and intrinsic factors (body size and feeding guild) on resource use and trophic position of fish consumers. Positive relationships between trophic position and body size were observed for zoobenthivore and piscivore fishes, whereas the relationship was negative for benthivore fishes. Body size is thus an important structuring mechanism in the systems. Trophic position decreased with increasing depth for all levels of biological organization. The amplitude of the change between shallow and deep stations was equivalent to more than one trophic level for generalist planktivores and piscivores. In the shallow English Channel, the food web is marked by stronger coupling of benthic and pelagic habitats via diverse pathways, due to the proximity of benthic and pelagic species, whereas in the Celtic Sea, increasing depth leads to a decoupling of benthic and pelagic pathways. For piscivores, a consistent pattern of increasing dependence on benthic subsidies with increasing size and depth highlights the importance of large consumers coupling energy across food web compartments. This study describes the relationship between production and trophic functioning and provides an empirical ecological explanation for cross‐ecosystem differences in observed trophic structures.