An organism’s survival depends on its ability to adequately respond to changes in internal and external conditions. When these changes are particularly demanding or life-threatening, they can act as stressors. In mammals, gut-associated microbial communities have been shown to be important modulators of host responses to external chronic stressors. However, the effects of internal or acute stressors on the gut microbiota are less well understood. Additionally, while most work has focused on community-level changes, how individual microbiota members evolve in response to stressors is yet to be investigated. In Chapter 1 of this dissertation, I explored how the gut microbiota of house mice (Mus musculus domesticus) responds to host internal stressors, specifically the metabolically demanding production of major urinary proteins (MUPs). I show that deletion of the Mup gene family caused sex-specific shifts in the taxonomic and functional composition of the mouse gut microbiota, including the depletion of microbes belonging to the Ruminococcaceae family, which has previously been shown to reduce the risk of metabolic disease. In Chapter 2, I investigated how the host and its gut microbiota respond to an acute external stressor (i.e., predator-odor exposure), comparing these responses to the effects of a well-established chronic stress paradigm (i.e., social isolation). I found that brief exposure to predator odor had a greater impact on the gut microbiota of wild-derived mice than prolonged social isolation, and that the gut microbiota was a better predictor of host behavior than was host gene expression. Finally, in Chapter 3, I explored how the host’s social environment affects the evolution of gut bacterial species. I found that social isolation accelerated divergent evolution in the native gut microbiota of wild-derived mice. The summation of this work contributes to our understanding of how gut symbionts shape the host’s ability to cope with diverse challenges.