Biotic gas generation from the degradation of organic carbon in marine sediments supplies and maintains gas hydrates throughout the world’s oceans. In nascent, ultraslow-spreading ocean basins, methane generation can also be abiotic, occurring during the high-temperature (>200 °C) serpentinization of ultramafic rocks. Here, we report on the evolution of a growing Arctic gas- and gas hydrate–charged sediment drift on oceanic crust in eastern Fram Strait, a tectonically controlled, deep-water gateway between the subpolar North Atlantic and Arctic Oceans. Ultraslow-spreading ridges between northwest Svalbard and northeast Greenland permit the sustained interaction of a mid-ocean ridge transform fault and developing sediment drift, on both young (<10 Ma) and old (>10 Ma) oceanic crust, since the late Miocene. Geophysical data image the gas-charged drift and crustal structure and constrain the timing of a major 30 km lateral displacement of the drift across the Molloy transform fault. We describe the buildup of a 2 m.y., long-lived gas hydrate– and free gas–charged drift system on young oceanic crust that may be fed and maintained by a dominantly abiotic methane source. Ultraslow-spreading, sedimented ridge flanks represent a previously unrecognized carbon reservoir for abiotic methane that could supply and maintain deep-water methane hydrate systems throughout the Arctic.