Arctic permafrost caps vast amounts of old, geologic methane (CH4) in subsurface reservoirs. Thawing permafrost opens pathways for this CH4 to migrate to the surface. However, the occurrence of geologic emissions and their contribution to the CH4 budget in addition to recent, biogenic CH4 is uncertain. Here we present a high-resolution (100 m × 100 m) regional (10,000 km²) CH4 flux map of the Mackenzie Delta, Canada, based on airborne CH4 flux data from July 2012 and 2013. We identify strong, likely geologic emissions solely where the permafrost is discontinuous. These peaks are 13 times larger than typical biogenic emissions. Whereas microbial CH4 production largely depends on recent air and soil temperature, geologic CH4 was produced over millions of years and can be released year-round provided open pathways exist. Therefore, even though they only occur on about 1% of the area, geologic hotspots contribute 17% to the annual CH4 emission estimate of our study area. We suggest that this share may increase if ongoing permafrost thaw opens new pathways. We conclude that, due to permafrost thaw, hydrocarbon-rich areas, prevalent in the Arctic, may see increased emission of geologic CH4 in the future, in addition to enhanced microbial CH4 production.