Abstract Oysters play an important role in coastal ecology and are a globally popular seafood source. However, their filter feeding lifestyle enables coastal pathogens, toxins, and pollutants to accumulate in their tissues, potentially endangering human health. For example, bacterial pathogens from both marine and terrestrial sources concentrate in oysters and can cause human illness when oysters are consumed raw. While pathogen concentrations in coastal waters are often linked to environmental conditions and runoff events, these do not always correlate with pathogen concentrations in oysters. Additional factors related to oyster hosts and the microbial ecology of pathogenic bacteria likely play a role in accumulation but are poorly understood. In this study, we investigated whether microbial communities in water and oysters were linked to accumulation of fecal indicators, Vibrio parahaemolyticus , and Vibrio vulnificus . Site-specific environmental conditions significantly influenced the composition and diversity of water microbial communities, which were linked to the highest concentrations of both Vibrio spp. and fecal indicator bacteria. Oyster microbial communities, however, were less impacted by environmental variability and exhibited less variability in microbial community diversity and accumulation of target bacteria. Instead, changes in specific microbial taxa in oyster and water samples, particularly in oyster digestive glands, were linked to elevated potential pathogens in oysters, especially V. parahaemolyticus . This included an increase in cyanobacteria in both water and oyster digestive gland microbial communities, which could represent an environmental vector for Vibrio spp. transport and decreased relative abundance of Mycoplasma and other key members of the oyster digestive gland microbiota. These findings suggest that host and microbial factors, in addition to environmental variables, may influence pathogen accumulation in oysters.