The North American boreal forest is a massive ecosystem, and its keystone herbivore is the snowshoe hare (Lepus americanus). Hares are exposed to considerable environmental extremes in diet and weather, food availability, and predation risk. Gut microbiomes have been suggested to facilitate adaptive animal responses to environmental change, but severe environmental challenges to homeostasis can also disrupt host-microbiome relationships. To better understand gut microbiome contributions to animal acclimation, we studied the fecal bacterial microbiome of wild hares across two types of extreme environmental change that are integral to their natural history: (1) seasonal transitions between summer and winter, and (2) changes over the ~10 year “boom-bust” population cycles that are characterized by shifting food resource availability and predation pressure. When compared to summer, hares in winter had lower bacterial richness and were depleted in twenty families (including Oxalobacteraceae and Christensenellaceae) but enriched for Ruminococcaceae (a family which contains plant fibre degrading microbiota) alongside nine other bacterial groups. Marked bacterial microbiome differences also occurred across phases of the population cycle. Bacterial microbiomes were lower in richness and compositionally distinct in the peak compared to the increase or decline phases of the population cycle. Direct measures of host physiology and diet quality (fecal fibre contents) most strongly supported food resource availability as a mechanism underlying phase-based differences in bacterial communities, but fecal fibre contents could not fully account for bacterial microbiome variation across phases.