ABSTRACT: 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 reef site and within-reef benthic characteristics. At three coral reefs in St. John U.S. Virgin Islands, we collected 60 ml seawater 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 overall reef site overwhelmingly shapes microbial community structure, while within-reef benthic cover surrounding sample locations has minimal influence. However, “ecospheres,” the small-scale effects of benthic cover directly under each sample, significantly explain as much as 12.1% of within-reef microbial variation and may even outweigh variation attributable to reef site alone. These findings provide new insights into fine-scale spatial variability in reef seawater microbiomes that are crucial for their use as indicators of microbialization and coral reef health.