Surface ocean methane concentrations are usually supersaturated relative to the methane concentrations in the atmosphere, even away from benthic cold seeps that pulse methane into the water column. This surface ocean methane is produced largely through aerobic cleavage of methane from methylphosphonates, with the released phosphate serving as a nutrient source.We measured mixed layer nutrient concentrations, methane concentration, C isotopic composition, and cycling rates, and methane cycling gene abundances along the U.S. Atlantic Margin and in the northern Gulf of Mexico. Methane production and consumption genes were ubiquitous in both areas. Mixed layer methane anomalies sometimes exceeded 100 nM. Methane oxidation (MOx) rates were between 10's-100's of pM/d. Potential methane production rates determined using ¹⁴C-labeled methylphosphonate were generally lower than MOx rates measured in parallel. The carbon isotopic composition of mixed layer methane was distinct from cold seep methane and suggestive of a methyl-group source, likely methylphosphonate. Cryptic methane cycling, with oxidation occurring in parallel with production, is widespread but rarely in sync, meaning that surface ocean methane is not in steady-state. The dynamic cycling of methane in the surface ocean is only beginning to be appreciated.