Within a single animal species, different morphs can allow for differential exploitation of foraging niches between populations, while sexual size dimorphism can provide each sex with access to different resources. Despite being potentially important agents of evolution, resource polymorphisms, and the way they operate in wild populations, remain poorly understood. In this study, we examine how trophic factors can select for different body sizes between populations and sexes in a diving endotherm. Dive depth and duration are positively related to body size in diving birds and mammals, a relationship explained by a lower mass-specific metabolic rate and greater oxygen stores in larger individuals. Based on this allometry, we predict that selection for exploiting resources situated at different depths can drive the evolution of body size in species of diving endotherms at the population and sexual level. To test this prediction, we studied the foraging ecology of Blue-eyed Shags, a group of cormorants with male-biased sexual size dimorphism from across the Southern Ocean. We found that mean body mass and relative difference in body mass between sexes varied by up to 77% and 107% between neighbouring colonies, respectively. Birds from colonies with larger individuals dived deeper than birds from colonies with smaller individuals, when accounting for sex. In parallel, males dived further offshore and deeper than females and the sexual difference in dive depth reflected the level of sexual size dimorphism at each colony. We argue that body size in this group of birds is under intense selection for diving to depths of profitable benthic prey patches and that, locally, sexual niche divergence selection can exaggerate the sexual size dimorphism of Blue-eyed Shags initially set up by sexual selection. Our findings suggest that trophic resources can select for important geographic micro-variability in body size between populations and sexes.