Bacteria drive energy fluxes and geochemical processes in estuarine sediments. Deposit-feeding invertebrates alter the structure and activity of microbial communities through sediment ingestion, gut passage, and defecation. The eastern mud snail, Ilyanassa obsoleta, is native to estuaries of the northwestern Atlantic, ranging from Nova Scotia, Canada, to Florida in the USA. Given extremely high densities, their deposit-feeding and locomotory activities exert ecological influence on other invertebrates and microbes. Our aim was to characterize the bacterial microbiome of this ‘keystone species’ and determine how its feeding alters the native bacterial microbiota. We gathered snails from both mudflat and sandflat habitats and collected their fresh fecal pellets in the laboratory. Dissection of these same snails allowed us to compare bacterial assemblages of ingested sediments, shell surfaces, gut sections (esophagus, stomach, intestine), and feces using DNA metabarcoding. Our findings indicate a diverse, resident gut microbiota. The stomach and intestines were dominated by bacteria of the genus Mycoplasma. Comparison of ingesta and feces revealed digestion of several bacterial taxa, introduction of gut residents during passage, in addition to unique bacterial taxa within the feces of unknown provenance. Our results demonstrate that I. obsoleta has the potential to modify microbial community structure in estuarine sediments.