In the Atlantic Arctic, bowhead whales (Balaena mysticetus) were nearly exterminated by European whalers between the seventeenth and nineteenth centuries. The collapse of the East Greenland-Svalbard-Barents Sea population, from an estimated 50 000 to a few hundred individuals, drastically reduced predation on mesozooplankton. Here, we tested the hypothesis that this event strongly favoured the demography of the little auk (Alle alle), a zooplanktivorous feeder competitor of bowhead whales and the most abundant seabird in the Arctic. To estimate the effect of bowhead whaling on little auk abundance, we modelled the trophic niche overlap between the two species using deterministic simulations of mesozooplankton spatial distribution. We estimated that bowhead whaling could have led to a 70% increase in northeast Atlantic Arctic little auk populations, from 2.8 to 4.8 million breeding pairs. While corresponding to a major population increase, this is far less than predicted by previous studies. Our study illustrates how a trophic shift can result from the near extirpation of a marine megafauna species, and the methodological framework we developed opens up new opportunities for marine trophic modelling.