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Abstract The Prairie Pothole Region (PPR) of North America contains millions of small depressional wetlands with some of the highest methane (CH₄) fluxes ever reported in terrestrial ecosystems. In saturated soils, two conventional paradigms are (a) methanogenesis is the final step in the redox ladder, occurring only after more thermodynamically favorable electron acceptors (e.g., sulfate) are reduced, and (b) CH₄is primarily produced by acetoclastic and hydrogenotrophic pathways. However, previous work in PPR wetlands observed co‐occurrence of sulfate‐reduction and methanogenesis and the presence of diverse methanogenic substrates (i.e., methanol, DMS). This study investigated how methylotrophic methanogenesis—in addition to acetoclastic and hydrogenotrophic methanogenesis—significantly contributes to CH₄flux in surface sediments and thus allows for the co‐occurrence of competing redox processes in PPR sediments. We addressed this aim through field studies in two distinct high CH₄emitting wetlands in the PPR complex, which coupled microbial community compositional and functional inferences with depth‐resolved electrochemistry measurements in surficial wetland sediments. This study revealed methylotrophic methanogens as the dominant group of methanogens in the presence of abundant organic sulfate esters, which are likely used for sulfate reduction. Resulting high sulfide concentrations likely caused sulfide toxicity in hydrogenotrophic and acetoclastic methanogens. Additionally, the use of non‐competitive substrates by many methylotrophic methanogens allows these metabolisms to bypass thermodynamic constraints and can explain co‐existence patterns of sulfate‐reduction and methanogenesis. This study demonstrates that the current models of methanogenesis in wetland ecosystems insufficiently represent carbon cycling in some of the highest CH₄emitting environments.