The Arctic Ocean subseabed holds vast reservoirs of the potent greenhouse gas methane (CH 4), often seeping into the ocean water column. In a continuously warming ocean as a result of climate change an increase of CH 4 seepage from the seabed is hypothesized. Today, CH 4 is largely retained in the water column due to the activity of methane-oxidizing bacteria (MOB) that thrive there. Predicted future oceanographic changes, bottom water warming and increasing CH 4 release may alter efficacy of this microbially mediated CH 4 sink. Here we investigate the composition and principle controls on abundance and activity of the MOB communities at the shallow continental shelf west of Svalbard, which is subject to strong seasonal changes in oceanographic conditions. Covering a large area (364 km 2), we measured vertical distribution of microbial methane oxidation (MOx) rates, MOB community composition, dissolved CH 4 concentrations, temperature and salinity four times throughout spring and summer during three consecutive years. Sequencing analyses of the pmoA gene revealed a small, relatively uniform community mainly composed of type-Ia methanotrophs (deep-sea 3 clade). We found highest MOx rates (7 nM d −1) in summer in bathymetric depressions filled with stagnant Atlantic Water containing moderate concentrations of dissolved CH 4 (< 100 nM). MOx rates in these depressions during spring were much lower (< 0.5 nM d −1) due to lower temperatures and mixing of Transformed Atlantic Water flushing MOB with the Atlantic Water out of the depressions. Our results show that MOB and MOx in CH 4-rich bottom waters are highly affected by geomorphology and seasonal conditions.