Permafrost soils store over half of global soil carbon (C), and northern frozen peatlands store about 10% of global permafrost C. With thaw, inundation of high latitude lowland peatlands typically increases the surface-atmosphere flux of methane (CH₄), a potent greenhouse gas. To examine the effects of lowland permafrost thaw over millennial timescales, we measured carbon dioxide (CO₂) and CH₄ exchange along sites that constitute a ~1000 yr thaw chronosequence of thermokarst collapse bogs and adjacent fen locations at Innoko Flats Wildlife Refuge in western Alaska. Peak CH₄exchange in July (123 ± 71 mg CH₄–C m⁻² d⁻¹) was observed in features that have been thawed for 30 to 70 (<100) yr, where soils were warmer than at more recently thawed sites (14 to 21 yr; emitting 1.37 ± 0.67 mg CH₄–C m⁻² d⁻¹ in July) and had shallower water tables than at older sites (200 to 1400 yr; emitting 6.55 ± 2.23 mg CH₄–C m⁻² d⁻¹ in July). Carbon lost via CH₄ efflux during the growing season at these intermediate age sites was 8% of uptake by net ecosystem exchange. Our results provide evidence that CH₄ emissions following lowland permafrost thaw are enhanced over decadal time scales, but limited over millennia. Over larger spatial scales, adjacent fen systems may contribute sustained CH₄ emission, CO₂ uptake, and DOC export. We argue that over timescales of decades to centuries, thaw features in high-latitude lowland peatlands, particularly those developed on poorly drained mineral substrates, are a key locus of elevated CH₄ emission to the atmosphere that must be considered for a complete understanding of high latitude CH₄ dynamics.