Free-ranging predator diet estimation is commonly achieved by applying molecular-based tracers because direct observation is not logistically feasible or robust. However, tracers typically do not represent all dietary macronutrients, which likely obscures resource use as prey proximate composition varies and tissue consumption can be specific. For example, polar bears (Ursus maritimus) preferentially consume blubber, yet diets have been estimated using fatty acids based on prey blubber or stable isotopes of lipid-extracted prey muscle, neither of which represent both protein and lipid macronutrient contributions. Further, additional bias can be introduced because dietary fat is known to be flexibly routed beyond short-term energy production and storage. We address this problem by simultaneously accounting for protein and lipid assimilation using carbon and nitrogen isotope compositions of lipid-containing prey muscle and blubber to infer summer/fall diet composition and macronutrient proportions from Chukchi Sea polar bear guard hair (n = 229) sampled each spring between 2008 and 2017. Inclusion of blubber (85–95% lipid by dry mass) expanded the isotope mixing space and improved separation among prey species. Ice-associated seals, including nutritionally dependent pups, were the primary prey in summer/fall diets with lower contributions by Pacific walruses (Odobenus rosmarus) and whales. Percent blubber estimates confirmed preferential selection of this tissue and represented the highest documented lipid assimilation for any animal species. Our results offer an improved understanding of summer/fall prey macronutrient usage by Chukchi Sea polar bears which likely coincides with a nutritional bottleneck as the sea ice minimum is approached.