The abundance, activity, and temperature response of aerobic methane-oxidizing bacteria were studied in permafrost-affected tundra soils of northeast Siberia. The soils were characterized by both a high accumulation of organic matter at the surface and high methane concentrations in the water-saturated soils. The methane oxidation rates of up to 835 nmol CH4 h−1 g−1 in the surface soils were similar to the highest values reported so far for natural wetland soils worldwide. The temperature response of methane oxidation was measured during short incubations and revealed maximum rates between 22 °C and 28 °C. The active methanotrophic community was characterized by its phospholipid fatty acid (PLFA) concentrations and with stable isotope probing (SIP). Concentrations of 16:1ω8 and 18:1ω8 PLFAs, specific to methanotrophic bacteria, correlated significantly with the potential methane oxidation rates. In all soils, distinct 16:1 PLFAs were dominant, indicating a predominance of type I methanotrophs. However, long-term incubation of soil samples at 0 °C and 22 °C demonstrated a shift in the composition of the active community with rising temperatures. At 0 °C, only the concentrations of 16:1 PLFAs increased and those of 18:1 PLFAs decreased, whereas the opposite was true at 22 °C. Similarly, SIP with 13CH4 showed a temperature-dependent pattern. When the soils were incubated at 0 °C, most of the incorporated label (83%) was found in 16:1 PLFAs and only 2% in 18:1 PLFAs. In soils incubated at 22 °C, almost equal amounts of 13C label were incorporated into 16:1 PLFAs and 18:1 PLFAs (33% and 36%, respectively). We concluded that the highly active methane-oxidizing community in cold permafrost-affected soils was dominated by type I methanotrophs under in situ conditions. However, rising temperatures, as predicted for the future, seem to increase the importance of type II methanotrophs, which may affect methane cycling in northern wetlands.