Methanotrophic bacteria are important soil biofilters for the climate-active gas methane. These bacteria grow exclusively by aerobic respiration of single-carbon and, in limited instances, short-chain hydrocarbons. However, the mechanisms that these specialists use to survive methane and oxygen limitation in their environment have remained elusive to now. Here we show that methanotrophic bacterium metabolise hydrogen gas (H2) during growth, methane-limitation, and oxygen-limitation. We isolated, sequenced, and characterised a verrucomicrobial methanotroph, Methylacidiphilum sp. RTK17.1, from a geothermal field in Rotokawa, New Zealand. The bacterium constitutively expressed a membrane-bound hydrogenase to aerobically respire H2 at environmentally significant concentrations. This process significantly enhanced mixotrophic growth yields of the bacterium, particularly under microoxic conditions, and was sustained in non-growing cultures starved for methane. We also observed that, under anoxic conditions, the bacterium maintained redox balance by coupling consumption of intracellular glycogen reserves to the fermentative evolution of H2. An environmental survey suggested that verrucomicrobial methanotrophs adopt a mixotrophic lifestyle in situ, leading them to become the dominant bacterial phylum in Rotokawa surface soils. We have identified genes encoding hydrogenases in all publicly-available methanotroph genomes, suggesting that aerobic H2 respiration and fermentative H2 evolution serve as general strategies for methanotrophs to remain energised in chemically-limited environments.