Aerobic methane oxidation is driven by both abiotic and biotic factors, which are often confounded in the soil environment. Using a laboratory-scale reciprocal inoculation experiment with two native soils (paddy and upland agricultural soils) and the gamma-irradiated fraction of these soils, we aim to disentangle and determine the relative contribution of abiotic (i.e., soil edaphic properties) and biotic (i.e., initial methanotrophic community composition) controls of methane oxidation during re-colonization. Methane uptake was appreciably higher in incubations containing gamma-irradiated paddy than upland soil despite the initial difference in the methanotrophic community composition. This suggested an overriding effect of the soil edaphic properties, which positively regulated methane oxidation. Community composition was similar in incubations with the same starting inoculum, based on quantitative and qualitative pmoA gene analyses. Thus, results suggested that the initial community composition affects the trajectory of community succession to an extent, but not at the expense of the methanotrophic activity under high methane availability. Still, methane oxidation was affected more by soil edaphic properties than by the initial composition of the methanotrophic community.