The permeable rocks of the upper oceanic basement contain seawater-sourced fluids estimated to be ~ 2% of the global ocean volume. This represents a very large potential subsurface biosphere supported by chemosynthesis. Recent collection of high integrity samples of basement fluid from the sedimented young basaltic basement on the Juan de Fuca Ridge flanks, off the coasts of Vancouver Island (Canada) and Washington (USA), and subsequent chemical analyses permit numerical modeling of metabolic redox reaction energetics. Here, values of Gibbs free energy for potential chemolithotrophic net reactions were calculated in basement fluid and in zones where basement fluid and entrained seawater may mix; the energy yields are reported both on a per mole electrons transferred and on a per kg of basement fluid basis. In pure basement fluid, energy yields from the anaerobic respiration processes investigated are anemic, releasing < 0.3 J/kg basement fluid for all reactions except methane oxidation by ferric iron, which releases ~ 0.6 J/kg basement fluid. In mixed solutions, aerobic oxidation of hydrogen, methane, and sulfide is the most exergonic on a per mole electron basis. Per kg of basement fluid, the aerobic oxidation of ammonia is by far the most exergonic at low temperature and high seawater:basement fluid ratio, decreasing by more than two orders of magnitude at the highest temperature (63 °C) and lowest seawater:basement fluid ratio investigated. Compared with mixing zones in deep-sea hydrothermal systems, oceanic basement aquifers appear to be very low energy systems, but because of their expanse, may support what has been labeled the ‘starving majority’.