Background: Changes in wild animal gut microbiotas may influence host health and fitness. While many studies have shown correlations between gut microbiota structure and external factors, few studies demonstrate causal links between environmental variables and microbiota shifts. Here, we use a fully factorial experiment to test the effects of elevated ambient temperature and natural nest parasitism by nest flies (Protocalliphora sialia) on the microbiotas of two species of wild birds, the eastern bluebird (Sialia sialis) and the tree swallow (Tachycineta bicolor).Results: We find that bacterial communities from the nestlings of each host species show differential response to both heat and parasitism, with gut microbiotas of eastern bluebirds more disrupted by heat and parasitism than those of tree swallows. Thus, we find that eastern bluebirds are unable to maintain stable associations with their gut bacteria in the face of both elevated temperature and parasitism. In contrast, tree swallow gut microbiotas are not significantly impacted by either heat or nest parasitism.Conclusions: Our results suggest that excess heat (e.g., as a result of climate change) may destabilize natural host-parasite-microbiota systems, with the potential to affect host fitness and survival in the anthropocene.