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The potential for molecular hydrogen () generated via serpentinization to fuel subsurface microbial ecosystems independent from photosynthesis has prompted biogeochemical investigations of serpentinization‐influenced fluids. However, investigations typically sample via surface seeps or open‐borehole pumping, which can mix chemically distinct waters from different depths. Depth‐indiscriminate sampling methods could thus hinder understanding of the spatial controls on nutrient availability for microbial life. To resolve distinct groundwaters in a low‐temperature serpentinizing environment, we deployed packers (tools that seal against borehole walls during pumping) in two‐deep, peridotite‐hosted wells in the Samail Ophiolite, Oman. Isolation and pumping of discrete intervals as deep astobelow ground level revealed multiple aquifers that ranged in pH from 8 to 11. Chemical analyses and 16S rRNA gene sequencing of deep, highly reactedgroundwaters bearing up to,methane () andsulfate () revealed an ecosystem dominated by Bacteria affiliated with the class Thermodesulfovibrionia, a group of chemolithoheterotrophs supported byoxidation coupled toreduction. In shallower, oxidizedgroundwaters, aerobic and denitrifying heterotrophs were relatively more abundant. Highandof(up toand, respectively) indicated microbialoxidation, particularly inwaters with evidence of mixing withwaters. This study demonstrates the power of spatially resolving groundwaters to probe their distinct geochemical conditions and chemosynthetic communities. Such information will help improve predictions of where microbial activity in fractured rock ecosystems might occur, including beyond Earth.