Climate-sensitive Arctic lakes have been identified as conduits for ancient permafrost-carbon (C) emissions and as such accelerate warming. However, the environmental factors that control emission pathways and their sources are unclear; this complicates upscaling, forecasting and climate-impact-assessment efforts. Here we show that current whole-lake CH4 and CO2 emissions from widespread lakes in Arctic Alaska primarily originate from organic matter fixed within the past 3-4 millennia (modern to 3,300 ± 70 years before the present), and not from Pleistocene permafrost C. Furthermore, almost 100% of the annual diffusive C flux is emitted as CO2. Although the lakes mostly processed younger C (89 ± 3% of total C emissions), minor contributions from ancient C sources were two times greater in fine-textured versus coarse-textured Pleistocene sediments, which emphasizes the importance of the underlying geological substrate in current and future emissions. This spatially extensive survey considered the environmental and temporal variability necessary to monitor and forecast the fate of ancient permafrost C as Arctic warming progresses.