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In Arctic regions, thawing permafrost soils are projected to release 50 to 250 Gt of carbon by 2100. This data is mostly derived from carbon-rich wetlands, although 71% of this carbon pool is stored in faster-thawing mineral soils, where ecosystems close to the outer boundaries of permafrost regions are especially vulnerable. Although extensive data exists from currently thawing sites and short-term thawing experiments, investigations of the long-term changes following final thaw and co-occurring drainage are scarce. Here we show ecosystem changes at two comparable tussock tundra sites with distinct permafrost thaw histories, representing 15 and 25 years of natural drainage, that resulted in a 10-fold decrease in CH4 emissions (3.2 ± 2.2 vs. 0.3 ± 0.4 mg C-CH4 m−2 day−1), while CO2 emissions were comparable. These data extend the time perspective from earlier studies based on short-term experimental drainage. The overall microbial community structures did not differ significantly between sites, although the drier top soils at the most advanced site led to a loss of methanogens and their syntrophic partners in surface layers while the abundance of methanotrophs remained unchanged. The resulting deeper aeration zones likely increased CH4 oxidation due to the longer residence time of CH4 in the oxidation zone, while the observed loss of aerenchyma plants reduced CH4 diffusion from deeper soil layers directly to the atmosphere. Our findings highlight the importance of including hydrological, vegetation and microbial specific responses when studying long-term effects of climate change on CH4 emissions and underscores the need for data from different soil types and thaw histories.