One third of the world’s soil carbon is sequestered in Arctic permafrost soils, which are thawing due to warming in the Arctic. Permafrost thaw allows microorganisms to access previously unavailable soil organic matter and emit CO2 and CH4 through decomposition. Since CH4 has 80-times the impact of CO2 on a 20-year timescale, the ratio of CO2:CH4 emissions determines the impact of permafrost decomposition on future warming. Microbial metabolisms, like methanogenesis and methanotrophy, can influence this ratio through production or consumption of methane. However, these microbes do not behave individually, instead relying on a network of metabolisms to feed them fermented carbon from complex organic matter. A holistic view of how microbial metabolic structures are changing with thaw is critical to predict future CO2:CH4 emissions. Here, we used shotgun metagenomic data to monitor the microbial community compositional and metabolic dynamics in active-layer soil over six years (2011 – 2017) along a permafrost thaw gradient—intact palsa, partially thawed bog and fully thawed fen—in Stordalen Mire, near Abisko, Sweden. Genome-centric analysis recovered 13,290 medium- to high-quality metagenome-assembled genomes (MAGs) representing 75% of the diversity at the genus level. Using a pathway-based approach, we defined the metabolic potential and the metabolic activity of carbon, nitrogen and sulfur cycling pathways for each MAG. Our work has identified several major differences in metabolic processes across the thaw stages, with only minor changes across years. Macromolecule and sugar degrading Acidobacteriota dominated the aerobic palsa, while hydrogenotrophic methanogens, fermenters and nitrogen fixers were highly active in the bog, increasing with depth and the aerobic-anaerobic transition. An additional population of proteobacterial methanotrophs decreased in abundance and activity with depth. In contrast, a highly diverse microbial community was active in the anaerobic fen, primarily acetoclastic methanogens. The thaw gradient maps a transition from aerobic to anaerobic degradation with increased methanogenesis and reduced methanotrophy, following the known increase in CH4 emissions. This study provides a description of the formation and stability of microbial metabolic structure in thawing permafrost that informs our understanding of the impact of permafrost thaw on future greenhouse gas emissions.