<p>Diet is a fundamental trait of fish that defines their roles in food webs and in regulating the functions of aquatic ecosystems. The role of evolutionary history, including conservatism and divergence, in diet shaping is poorly understood, especially for fish living in marine ecosystems such as seagrass beds. Using a series of phylogenetic comparative analyses, we investigate conservatism and divergence in the diet of fishes associated with seagrass beds globally over deep evolutionary time. We find that the trophic levels of seagrass bed fishes exhibit a strong phylogenetic pattern, with closely related fishes being more trophically similar. This phylogenetic pattern is also supported by macroevolutionary model inferences, with major diet divergences occurring deep in history. Consistently, phylogenetic relationships explain ~ 60% of the variation in the diet composition of seagrass bed fishes, whereas contemporary morphological, ecological, and geographical factors explain ~ 5% in total. These results reveal that the diet of seagrass bed fishes has been shaped by general conservatism, with rare divergences leading to abrupt diet shifts. Our study fills a key gap in understanding the shaping of fish diet in seagrass beds and suggests that diet specialists represent products of long-term evolution and have irreplaceable functions, warranting priority conservation.</p>