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 (¹⁴C_CH4 20 079 ± 1227 years BP, mean ± standard error (s.e.m.) years) to deeper taliks (thaw bulbs) compared to younger ¹⁴C_CH4 in new lakes (¹⁴C_CH4 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.