Seawater microorganisms impact ecological and biogeochemical cycling on coral reefs and are sensitive indicators of ecosystem status. Microbialization, a shift towards trophic collapse and higher microbial biomass on coral reefs, is a global concern. Indeed, macro organisms can influence microbial processes and community composition on reefs, which is best understood as increased macroalgae resulting in copiotrophic microbial growth and oxygen reduction. Whether or not smaller scale changes in macro organisms influence the overlying seawater microbial communities is largely unknown. Here, we assessed seawater microorganisms across three coral reefs to understand their connection to site-specific benthic characteristics. At three coral reefs in St. John U.S. Virgin Islands, we collected 60 ml samples 2 cm above the seafloor, spaced 2 m apart in a grid pattern, and assessed bacterial and archaeal communities via sequencing of small subunit ribosomal RNA genes. Benthic cover within 1 m of each sample was determined at 10 cm resolution through photogrammetry. Our results reveal that reef site or location overwhelmingly shapes microbial community structure, while surrounding benthic cover has minimal influence. However, "ecospheres," the small-scale effects of organisms directly under each sample, significantly explain intra-site microbial variation but patterns of these associations differ between sites. Remarkably, over half of microbial community variation remains unexplained by site, benthic cover, or organismal effects. These findings provide new insights into fine-scale variability in reef seawater microbiomes that are crucial for their use as indicators of microbialization and coral reef health.