The most climate-sensitive methane hydrate deposits occur on upper continental slopes at depths close to the minimum pressure and maximum temperature for gas hydrate stability. At these water depths, small perturbations in intermediate ocean water temperatures can lead to gas hydrate dissociation. The Arctic Ocean has experienced more dramatic warming than lower latitudes, but observational data have not been used to study the interplay between upper slope gas hydrates and warming ocean waters. Here we use (a) legacy seismic data that constrain upper slope gas hydrate distributions on the U.S. Beaufort Sea margin, (b) Alaskan North Slope borehole data and offshore thermal gradients determined from gas hydrate stability zone thickness to infer regional heat flow, and (c) 1088 direct measurements to characterize multidecadal intermediate ocean warming in the U.S. Beaufort Sea. Combining these data with a three-dimensional thermal model shows that the observed gas hydrate stability zone is too deep by 100 to 250 m. The disparity can be partially attributed to several processes, but the most important is the reequilibration (thinning) of gas hydrates in response to significant (~0.5°C at 2σ certainty) warming of intermediate ocean temperatures over 39 years in a depth range that brackets the upper slope extent of the gas hydrate stability zone. Even in the absence of additional ocean warming, 0.44 to 2.2 Gt of methane could be released from reequilibrating gas hydrates into the sediments underlying an area of ~5–7.5 × 10³ km² on the U.S. Beaufort Sea upper slope during the next century.