In this study, we report evidence that temperature plays a key role in determining the relative abundance of two mutualistic fungi associated with an economically and ecologically important bark beetle, Dendroctonus ponderosae. The symbiotic fungi possess different optimal temperature ranges. These differences determine which fungus is vectored by dispersing host beetles as temperatures fluctuate over a season. Grosmannia clavigera is the predominant fungus carried by dispersing beetles during cool periods but decreases in prevalence as daily maximum temperatures approach 25°C, and becomes extremely rare when temperatures reach or exceed 32°C. In contrast, Ophiostoma montium increases in prevalence as temperatures approach 25°C, and becomes the predominant symbiont dispersed when temperatures reach or exceed 32°C. The possession of different optimal growth temperatures may facilitate the stable coexistence of the two fungi by supporting growth of each fungus at different times, minimizing direct competition. Furthermore, the beetle may reduce its risk of being left aposymbiotic by exploiting not one, but two symbionts, whose combined growth optima span a wide range of environmental conditions. The possession of multiple symbionts with different temperature tolerances may allow the beetle to occupy highly variable habitats over a wide geographic range. Such temperature-driven symbiont shifts are likely to have major consequences for both the host and its symbionts under current temperature regimes and those predicted to occur because of climate change.