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ABSTRACT Niche partitioning promotes species coexistence. Yet, it remains unclear how phylogeny and morphology influence the trophic niches of closely related aquatic species with shared feeding modes. Freshwater mussels (Family: Unionidae) are a group of filter‐feeding bivalves that are ideal for investigating mechanisms of niche partitioning. Particle size selection and patterns of ingestion are controlled by gill latero‐frontal cirri density (CD) and the number of cilia per cirrus (CC). We investigated trophic assimilation and niche area using stable isotope signatures (𝛿¹³C and 𝛿¹⁵N) and gill morphology with scanning‐electron microscopy for a diverse mussel assemblage from the Sipsey River, Alabama, USA. We predicted that (1) trophic niches and gill morphology would differ within and among species across sites; (2) co‐occurring species would partition food resources; (3) greater phylogenetic distances among species would result in increased trophic dissimilarity; (4) more CC and higher CD would result in a narrower trophic niche area, or more constrained range of food items assimilated. We found that (1) species identity and site influenced gill morphology and stable isotope signatures but that the trophic niche area of a species was only affected by species identity; (2) the average proportion of niche area overlap between co‐occurring species was low across sites (0.04 to 0.18); (3) trophic dissimilarity among species increased with phylogenetic distance; (4) CD but not the number of CC negatively related to trophic niche area. Our results indicate that gill morphology and evolutionary history are likely key factors governing the trophic niches of mussels. In addition, intraspecific variation in gill morphology across sites may either reflect a phenotypic response to differences in local resource availability or suggest that other mechanisms shape particle selection. Examining the interplay among the trophic niche, phylogeny, and morphology among functionally similar species further informs our understanding of the mechanisms facilitating their coexistence.