Anaerobic oxidation of methane (AOM) coupled with sulphate reduction (SR) is a crucial microbial process that mitigates methane emissions, a major contributor to climate change. However, the bioenergetics underlying this process remains poorly understood. Here, we present a metabolic model to quantify energy fluxes and conservation in AOM consortia by integrating enzyme-level thermodynamics and kinetics. Unlike previous models that impose artificial constraints on energy conservation kinetics and efficiency, our approach mechanistically predicts ATP yields and energy efficiencies. We show that both anaerobic methanotrophic archaea (ANME) and sulphate-reducing bacteria (SRB) invest energy in substrate activation, synthesising ATP with comparable yields (0.23-0.24 mol ATP per mol methane or sulphate), while achieving remarkable thermodynamic efficiency (~60%). However, ANME exhibit a higher return on investment (ROI, 18%) than SRB (11%) due to more efficient substrate activation. These findings highlight fundamental bioenergetic constraints governing methane oxidation and SR in anoxic environments, enhancing our understanding of how microbial processes regulate methane fluxes in natural ecosystems. By providing a quantitative framework for microbial energy conservation, our study advances biogeochemical modelling and informs strategies for methane mitigation in marine sediments and other anaerobic environments critical to climate regulation.