Methanogenesis has traditionally been assumed to occur only in anoxic environments, yet there is mounting, albeit indirect, evidence of methane (CH4) production in oxic marine and freshwaters. Here we present the first direct, ecosystem-scale demonstration of methanogenesis in oxic lake waters. This methanogenesis appears to be driven by acetoclastic production, and is closely linked to algal dynamics. We show that oxic water methanogenesis is a significant component of the overall CH4 budget in a small, shallow lake, and provide evidence that this pathway may be the main CH4 source in large, deep lakes and open oceans. Our results challenge the current global understanding of aquatic CH4 dynamics, and suggest a hitherto unestablished link between pelagic CH4 emissions and surface-water primary production. This link may be particularly sensitive to widespread and increasing human influences on aquatic ecosystem primary productivity.