The Sierra Nevada red fox (SNRF; Vulpes vulpes necator) is an endangered subspecies restricted to high-elevation habitats. Competition with larger-bodied coyotes (Canis latrans) limits red fox abundance throughout their sympatric ranges. Because SNRF were isolated and have evolved solely within subalpine ecosystems, we hypothesized that specialized adaptations, including low foot loading to more efficiently hunt snow-adapted lagomorphs in deep snow conditions, facilitate coexistence with coyotes. Because subalpine lagomorphs are themselves in decline, understanding the contribution of these and other prey to the SNRF diet and those of coyotes and other sympatric mesocarnivores is fundamental to SNRF conservation. We used metabarcoding to investigate the diets and niche relationships of these carnivores, along with martens (Martes caurina) and bobcats (Lynx rufus) using 789 scats collected from sites of two SNRF populations (Lassen, Sierra Nevada). As predicted, SNRFs exhibited high dietary overlap with coyotes but showed greater specialization for white-tailed jackrabbits (Lepus townsendii) and American pika (Ochotona princeps). In both populations, SNRF diet consisted primarily of small rodents and lagomorphs. Dietary overlap was higher with coyotes (Pianka’s index: 0.89) than with martens (0.56) and bobcats (0.59). SNRFs more frequently than coyotes consumed lagomorphs (p ≤ 0.005). We also observed a high frequency of pine, most likely whitebark pine (Pinus albicaulus) seeds, in SNRF scats, particularly during winter. Our findings suggest that subalpine specialist prey species may play a major role in facilitating SNRF coexistence with coyotes, and underscore the need for data on the current status and trends of these sensitive lagomorph populations.