Niche overlap between native species and ecologically similar invaders can lead to competitive exclusion of threatened native species, but if two such species also co‐occur naturally elsewhere, interactions between native and introduced populations may mirror coevolved niche partitioning that reduces competition and promotes coexistence. A single, insular population of Fremont’s squirrel (Tamiasciurus fremonti) the Mount Graham red squirrel (MGRS; T. f. grahamensis) in the Pinaleño Mountains, Arizona, USA, is critically endangered and resource competition with introduced Abert’s squirrels (Sciurus aberti) may threaten its long‐term persistence. The species are naturally synoptic in other mountain sites, and both consume diets comprised primarily of conifer seeds and fungi. We conducted experimental removals of introduced Abert’s squirrels and used stable isotope analysis of diets before and after removals, and of diets in naturally syntopic populations to test the hypothesis that dietary niche partitioning can facilitate coexistence between native and introduced species. We also developed a novel approach to determine the influence of fluctuating food availability on carbon enrichment in consumers. Mount Graham red squirrels and introduced Abert’s squirrels partitioned the dietary niche similarly to naturally syntopic populations. Removals had no apparent effect. Diet of MGRS was more closely linked to availability of resources than to presence of Abert’s squirrels. Flexible dietary niche of introduced Abert’s squirrels may have allowed them to exploit a resource opportunity in syntopy with MGRS. Variable food production of MGRS habitat may intensify competition in poor years, and territorial defense against non‐native Abert’s squirrels likely imposes fitness costs on individual MGRS. Similarity in our model species’ diets may make MGRS more vulnerable to competition if climate change eliminates the advantages of larder‐hoarding. Where introduced populations of ecologically similar species are better adapted to changing conditions, they may ultimately replace southern peripheral populations of native species.