Recent field studies have documented a surprisingly strong and consistent methane sink in arctic mineral soils, thought to be due to high-affinity methanotrophy. However, the distinctive physiology of these methanotrophs is poorly represented in mechanistic methane models. We developed a new model, constrained by microcosm experiments, to simulate the activity of high-affinity methanotrophs. The model was tested against soil core-thawing experiments and field-based measurements of methane fluxes and was compared to conventional mechanistic methane models. Our simulations show that high-affinity methanotrophy can be an important component of the net methane flux from arctic mineral soils. Simulations without this process overestimate methane emissions. Furthermore, simulations of methane flux seasonality are improved by dynamic simulation of active microbial biomass. Because a large fraction of the Arctic is characterized by mineral soils, high-affinity methanotrophy will likely have a strong effect on its net methane flux. ©2016. American Geophysical Union. All Rights Reserved.