Methane emissions from the sea floor affect methane inputs into the atmosphere, ocean acidification and de-oxygenation, the distribution of chemosynthetic communities and energy resources. Global methane flux from seabed cold seeps has only been estimated for continental shelves, at 8 to 65 Tg CH₄ yr⁻¹, yet other parts of marine continental margins are also emitting methane. The US Atlantic margin has not been considered an area of widespread seepage, with only three methane seeps recognized seaward of the shelf break. However, massive upper-slope seepage related to gas hydrate degradation has been predicted for the southern part of this margin, even though this process has previously only been recognized in the Arctic. Here we use multibeam water-column backscatter data that cover 94,000 km² of sea floor to identify about 570 gas plumes at water depths between 50 and 1,700 m between Cape Hatteras and Georges Bank on the northern US Atlantic passive margin. About 440 seeps originate at water depths that bracket the updip limit for methane hydrate stability. Contemporary upper-slope seepage there may be triggered by ongoing warming of intermediate waters, but authigenic carbonates observed imply that emissions have continued for more than 1,000 years at some seeps. Extrapolating the upper-slope seep density on this margin to the global passive margin system, we suggest that tens of thousands of seeps could be discoverable.