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Gut microbiomes are increasingly recognized for mediating diverse biological aspects of their hosts, including complex behavioral phenotypes. Although many studies have reported that experimental disruptions to the gut microbial community result in atypical host behavior, studies that address how gut microbes contribute to adaptive behavioral trait variation are rare. Eusocial insects represent a powerful model to test this, because of their simple gut microbiota and complex division of labor characterized by colony-level variation in behavioral phenotypes. Although previous studies report correlational differences in gut microbial community associated with division of labor, here, we provide evidence that gut microbes play a causal role in defining differences in foraging behavior between European honey bees (Apis mellifera). We found that gut microbial community structure differed between hive-based nurse bees and bees that leave the hive to forage for floral resources. These differences were associated with variation in the abundance of individual microbes, including Bifidobacterium asteroides, Bombilactobacillus mellis, and Lactobacillus melliventris. Manipulations of colony demography and individual foraging experience suggested that differences in gut microbial community composition were associated with task experience. Moreover, single-microbe inoculations with B. asteroides, B. mellis, and L. melliventris caused effects on foraging intensity. These results demonstrate that gut microbes contribute to division of labor in a social insect, and support a role of gut microbes in modulating host behavioral trait variation., (© The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.)