Methane (CH₄) emissions from climate-sensitive ecosystems within the northern permafrost region represent a large but highly uncertain source, with current estimates spanning a factor of seven (11 – 75 Tg CH₄ yr^-1). Accelerating permafrost thaw threatens significant increases in pan-Arctic CH₄ emissions, amplifying the permafrost carbon feedback. We used airborne imaging spectroscopy with meter-scale spatial resolution and broad coverage to identify a previously undiscovered CH₄ hotspot adjacent to an intensively studied thermokarst lake in interior Alaska. Hotspot emissions were confined to < 1% of the 10 ha study area. Ground-based chamber measurements confirmed average daily fluxes of 1,170 mg CH₄ m^-2 d^-1, with extreme daily maxima up to 24,200 mg CH₄ m^-2 d^-1. Ground-based geophysics measurements revealed thawed permafrost at and directly beneath the CH₄ hotspot, extending to a depth of ~15 m, indicating that the intense CH₄ emissions likely originated from recently thawed permafrost. Emissions from the hotspot accounted for ~40% of total diffusive CH₄ emissions from the entire study area. Combining these results with hotspot statistics from our 70,000 km² airborne survey across Alaska and northwestern Canada, we estimate that terrestrial thermokarst hotspots currently emit 1.1 (0.1 – 5.2) Tg CH₄ yr^-1, or roughly 4% of the annual pan-Arctic wetland budget from just 0.01% of the northern permafrost land area. Our results suggest that significant proportions of pan-Arctic CH₄ emissions originate from disproportionately small areas of previously undetermined thermokarst emissions hotspots, and that pan-Arctic CH₄ emissions may increase non-linearly as thermokarst processes increase under a warming climate.