Methane, a potent greenhouse gas, accumulates in subsurface hydrocarbon reservoirs. In the Arctic, impermeable icy permafrost and glacial overburden form a ‘cryosphere cap’ that traps gas leaking from these reservoirs, restricting flow to the atmosphere. We document the release of geologic methane to the atmosphere from abundant gas seeps concentrated along boundaries of permafrost thaw and receding glaciers in Alaska. Through aerial and ground surveys we mapped >150,000 seeps identified as bubbling-induced open holes in lake ice. Subcap methane seeps had anomalously high fluxes, 14C-depletion, and stable isotope values matching known coalbed and thermogenic methane accumulations in Alaska. Additionally, we observed younger subcap methane seeps in Greenland that were associated with ice-sheet retreat since the Little Ice Age. These correlations suggest that in a warming climate, continued disintegration of permafrost, glaciers, and parts of the polar ice sheets will relax pressure on subsurface seals and further open conduits, allowing a transient expulsion of geologic methane currently trapped by the cryosphere cap.