Animals evolved in a microbial world, and their gut microbial symbionts have played a role in their ecological diversification. While many recent studies have reported patterns of co-diversification of hosts and their gut microbes, few studies have directly examined the functional contributions of these microbes to the dietary habits of their hosts. Here, we examined functional enrichment of metabolic pathways in the gut bacteria of 545 bats belonging to 60 species and five terrestrial feeding niches. We found that hosts of different dietary guilds had differential enrichment of bacterial functions that may be adaptive to their respective diets, and that metagenome functions were highly predictive of host feeding guild. We detected little evidence of host phylogenetic effect on gut metagenome composition, suggesting that diet likely overrides host evolutionary history in structuring functional pathways in the gut metagenome. Our results further suggest that bats may have evolved to partially rely on their gut microbes to fulfill critical metabolic pathways, including essential amino acid synthesis, fatty acid biosynthesis, and the generation of cofactors and vitamins essential for proper nutrition. This work represents a comprehensive and novel insight into the contribution of gut microbes to vital metabolic processes in a diverse Order of wild mammals.