Causes and consequences of differences in seabird foraging strategies between breeding colonies are not well understood. We tested whether body size of a pursuit-diving seabird, the thick-billed murre Uria lomvia, differs between breeding colonies and, if so, how size differences can be understood in the context of differences in foraging behavior, habitat use, and breeding performance. We measured adult murres over 3 seasons (2008 to 2010) at 2 of the Pribilof Islands, St. Paul and St. George, located on the continental shelf of the Bering Sea at different distances from the shelf break. Body mass and size were positively associated with deep diving and negatively associated with long flights, suggesting morphology influences foraging and commuting efficiency. Murres from St. Paul (farther from the shelf break) were larger than those from St. George (nearer the shelf break), foraged exclusively in the middle shelf domain, made deep dives during daylight, and fed on larger benthic prey. In contrast, smaller murres from St. George commuted greater distances to beyond the shelf break, made shallow dives at night, and fed on smaller, high-energy, schooling, vertical-migrating prey. Both foraging strategies resulted in similar chick-feeding rates and fledging success. The largest and the smallest murres experienced less stress during breeding compared to intermediate-sized murres, suggesting divergent selection for body size between islands. Nesting murres, as central-place foragers, may experience strong selection pressure on body size and other adaptive traits that reflect differences between breeding colonies in foraging ecology and the acquisition of resources for reproduction.