Aerobic methanotrophy has evolved in the biosphere more than once. Studies of aerobic methanotrophy have focused on two proteins: particulate methane monooxygenase (pMMO) and soluble methane monooxygenase (sMMO). Laboratory experiments and natural mesocosms, however, indicate that a broader range of proteins is capable of oxidizing methane and other small hydrocarbons in the environment, even at low substrate concentrations. Across a series of field expeditions in Alaska and California, we have measured methane gas fluxes in a variety of landscapes, including rivers, permafrost, desert, oak woodland, and arid rangeland. These environments encompass a wide range of temperature (subzero to > 40 ºC), moisture, and methane concentration conditions. Alaska riverine methane concentrations are substantial, in some cases surpassing deep sea methane concentrations near methane seeps. Across this variety of landscapes and conditions, we observe significant soil methanotrophy—even at and below atmospheric concentrations of methane (ca. 2 ppm). Using amplicon-based soil and water microbial community composition, metagenomic analyses, and laboratory experiments, we provide new insights into the range of metalloproteins that may be able to accomplish methanotrophy across a wide variety of environments.