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Abstract Microbial symbionts can influence their hosts in stunningly diverse ways. Emerging research suggests that an underappreciated facet of these relationships is the influence microbes can have on their host's responses to novel, or stressful, environmental conditions. We sought to address these and related questions in populations resulting from the recent introduction and subsequent rapid range expansion ofOnthophagus taurusdung beetles. Specifically, we manipulated both microbial communities and rearing temperature to detect signatures of developmental and life history differentiation in response to the local thermal conditions in two populations derived from the southern most (Florida) and northern most (Michigan) extremes of the exotic Eastern U.S. range ofO. taurus. We then sought to determine the contributions, if any, of host‐associated microbiota to this differentiation. We found that when reared under common garden conditions individuals from Florida and Michigan populations differed significantly in developmental performance measures and life history traits, consistent with population divergence. At the same time, and contrary to our predictions, we failed to find support for the hypothesis that animals perform better if reared at temperatures that match their location of origin and that performance differences may be mediated by host‐associated microbiota. Instead, we found that microbiome swapping across host populations improved developmental performance in both populations, consistent with enemy release dynamics. We discuss the implications of our results for our understanding of the rapid spread of exoticO. taurusthrough the Eastern United States and the significance of symbiosis in host responses to novel environmental conditions more broadly.