Hydrogen sulfide (H2S) is produced in a wide range of anoxic environments where sulfate (SO42−) reduction is coupled to decomposition of organic matter. In the same environments, methane (CH4) is the end product of an anaerobic food chain and both H2S and CH4 diffuse upwards into oxic zones where aerobic microorganisms can utilize these gases. Methane-oxidizing bacteria are known to oxidize a major part of the produced CH4 in these ecosystems, mitigating the emissions of this potent greenhouse gas to the atmosphere. However, how methanotrophy is affected by toxic H2S is largely unexplored. Here, we show that a single microorganism can oxidize CH4 and H2S simultaneously. By oxidizing H2S, the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV can alleviate the inhibitory effects on CH4 oxidation. In response to H2S, strain SolV upregulated a type III sulfide:quinone oxidoreductase (SQR) and a sulfide-insensitive ba3-type terminal oxidase to dissipate the reducing equivalents derived from H2S oxidation. Through extensive chemostat cultivation of M. fumariolicum SolV we demonstrate that it converts high loads of H2S to elemental sulfur (S0). Moreover, we show chemolithoautotrophy by tracing 13CO2 fixation into new biomass by using H2S as sole energy source. Molecular surveys revealed several putative SQR sequences in a range of proteobacterial methanotrophs from various environments, suggesting that H2S detoxification is much more widespread in methanotrophs than previously assumed, enabling them to connect carbon and sulfur cycles in new ways.