Thermokarst lakes accelerate deep permafrost thaw and the mobilization of previously frozen soil organic carbon. This leads to microbial decomposition and large releases of carbon dioxide (CO2) and methane (CH4) that enhance climate warming. However, the time scale of permafrost-carbon emissions following thaw is not well known but is important for understanding how abrupt permafrost thaw impacts climate feedback. We combined field measurements and radiocarbon dating of CH4 ebullition with (a) an assessment of lake area changes delineated from high-resolution (1–2.5 m) optical imagery and (b) geophysical measurements of thaw bulbs (taliks) to determine the spatiotemporal dynamics of hotspot-seep CH4 ebullition in interior Alaska thermokarst lakes. Hotspot seeps are characterized as point-sources of high ebullition that release 14C-depleted CH4 from deep (up to tens of meters) within lake thaw bulbs year-round. Thermokarst lakes, initiated by a variety of factors, doubled in number and increased 37.5% in area from 1949 to 2009 as climate warmed. Approximately 80% of contemporary CH4 hotspot seeps were associated with this recent thermokarst activity, occurring where 60 years of abrupt thaw took place as a result of new and expanded lake areas. Hotspot occurrence diminished with distance from thermokarst lake margins. We attribute older 14C ages of CH4 released from hotspot seeps in older, expanding thermokarst lakes (14CCH4 20 079 ± 1227 years BP, mean ± standard error (s.e.m.) years) to deeper taliks (thaw bulbs) compared to younger 14CCH4 in new lakes (14CCH4 8526 ± 741 years BP) with shallower taliks. We find that smaller, non-hotspot ebullition seeps have younger 14C ages (expanding lakes 7473 ± 1762 years; new lakes 4742 ± 803 years) and that their emissions span a larger historic range. These observations provide a first-order constraint on the magnitude and decadal-scale duration of CH4-hotspot seep emissions following formation of thermokarst lakes as climate warms.