Significance Much of Earth’s volcanism occurs in the deep sea, yet little is known about the microbial communities inhabiting such extreme and dynamic systems. Using a multidisciplinary approach to study distinct hydrothermal systems at Brothers submarine arc volcano, we provide insights into how microbial community composition and function reflect subtly different fluid chemistries resulting from subsurface fluid interactions with distinct alteration mineral assemblages. These variations can be traced to the subsurface hydrogeologic history beneath Brothers volcano. Further, we show that these systems represent oases of phylogenetically diverse Archaea and Bacteria. Our findings highlight the importance of geologic legacy in understanding drivers of microbial diversity, assembly, and evolution and may have insights into processes that drove early diversification of life on Earth.