Congeneric species often share ecological niche space resulting in competitive interactions that either limit co-occurrence or lead to niche partitioning. Differences in fundamental nutritional niches mediated through character displacement or isolation during evolution are potential mechanisms that could explain overlapping distribution patterns of congenerics. We directly compared nutritional requirements and tolerances that influence the fundamental niche of mule (Odocoileus hemionus) and white-tailed deer (O. virginianus), which occur in allopatry and sympatry in similar realized ecological niches across their ranges in North America. Digestible energy and protein requirements and tolerances for plant fiber and plant secondary metabolites (PSMs) of both deer species were quantified using in vivo digestion and intake tolerance trials with six diets ranging in content of fiber, protein, and PSMs using tractable deer raised under identical conditions in captivity. We found that compared with white-tailed deer, mule deer required 54% less digestible protein and 21% less digestible energy intake per day to maintain body mass and nitrogen balance. In addition, they had higher fiber, energy, and dry matter digestibility and produced glucuronic acid (a byproduct of PSM detoxification) at a slower rate when consuming the monoterpene α-pinene. The mule deers' enhanced physiological abilities to cope with low-quality, chemically defended forages relative to white-tailed deer might minimize potential competitive interactions in shared landscapes and provide a modest advantage to mule deer in habitats dominated by low-quality forages.