Termites are responsible for ∼1 to 3% of global methane (CH(4)) emissions. However, estimates of global termite CH(4) emissions span two orders of magnitude, suggesting that fundamental knowledge of CH(4) turnover processes in termite colonies is missing. In particular, there is little reliable information on the extent and location of microbial CH(4) oxidation in termite mounds. Here, we use a one-box model to unify three independent field methods—a gas-tracer test, an inhibitor approach, and a stable-isotope technique—and quantify CH(4) production, oxidation, and transport in three North Australian termite species with different feeding habits and mound architectures. We present systematic in situ evidence of widespread CH(4) oxidation in termite mounds, with 20 to 80% of termite-produced CH(4) being mitigated before emission to the atmosphere. Furthermore, closing the CH(4) mass balance in mounds allows us to estimate in situ termite biomass from CH(4) turnover, with mean biomass ranging between 22 and 86 g of termites per kilogram of mound for the three species. Field tests with excavated mounds show that the predominant location of CH(4) oxidation is either in the mound material or the soil beneath and is related to species-specific mound porosities. Regardless of termite species, however, our data and model suggest that the fraction of oxidized CH(4) (f(ox)) remains well buffered due to links among consumption, oxidation, and transport processes via mound CH(4) concentration. The mean f(ox) of 0.50 ± 0.11 (95% CI) from in situ measurements therefore presents a valid oxidation factor for future global estimates of termite CH(4) emissions.