Understanding how species partition the niche is a fundamental question in ecology. It is now also a critical question given the rapid pace of species extinctions in nature and the impact of biodiversity loss on ecosystem function. Niche partitioning may be especially complex for large, mobile fauna where the niche is partitioned across many axes such as body size, diet, and habitat. Here, we show the intestinal microbiome is an underappreciated axis of niche differentiation for herbivorous coral reef fishes, a group of consumers critical for the resilience of coral reefs. Our data show that these herbivores finely partition their dietary niche, a well-known phenomenon. However, differences among species are even more pronounced when considering the composition of their microbiome. Molecular analyses indicate those microbial taxa that are differentially abundant among herbivores are probably host-specific, and have convergently evolved over millions of years in related fishes across the globe. Microbes may thus underpin some of the functional diversity displayed by this important guild of consumers.