Nitrogen (N) deposition rates are increasing globally due to anthropogenic activities. Plant community responses to N are often attributed to altered competitive interactions between plants, but may also be a result of microbial responses to N, particularly root-associated fungi (RAF), which are known to affect plant fitness. In response to N, Deschampsia cespitosa, a codominant plant in the alpine tundra at Niwot Ridge (CO), increases in abundance, while Geum rossii, its principal competitor, declines. Importantly, G. rossii declines with N even in the absence of its competitor. We examined whether contrasting host responses to N are associated with altered plant–fungal symbioses, and whether the effects of N are distinct from effects of altered plant competition on RAF, using 454 pyrosequencing. Host RAF communities were distinct (only 9.4% of OTUs overlapped). N increased RAF diversity in G. rossii, but decreased it in D. cespitosa. D. cespitosa RAF communities were more responsive to N than G. rossii RAF communities, perhaps indicating a flexible microbial community aids host adaptation to nutrient enrichment. Effects of removing D. cespitosa were distinct from effects of N on G. rossii RAF, and D. cespitosa presence reversed RAF diversity response to N. The most dominant G. rossii RAF order, Helotiales, was the most affected by N, declining from 83% to 60% of sequences, perhaps indicating a loss of mutualists under N enrichment. These results highlight the potential importance of belowground microbial dynamics in plant responses to N deposition.