The expansive plains of West Siberia contain globally significant carbon stocks, with Earth's most extensive peatland complex overlying the world's largest‐known hydrocarbon basin. Numerous terrestrial methane seeps have recently been discovered on this landscape, located along the floodplains of the Ob and Irtysh Rivers in hotspots covering more than 2500 km2. We articulated three hypotheses to explain the origin and migration pathways of methane within these seeps: (H1) uplift of Cretaceous‐aged methane from deep petroleum reservoirs along faults and fractures, (H2) release of Oligocene‐aged methane capped or trapped by degrading permafrost, and (H3) horizontal migration of Holocene‐aged methane from surrounding peatlands. We tested these hypotheses using a range of geochemical tools on gas and water samples extracted from seeps, peatlands, and aquifers across the 120,000 km2 study area. Seep‐gas composition, radiocarbon age, and stable isotope fingerprints favor the peatland hypothesis of seep‐methane origin (H3). Organic matter in raised bogs is the primary source of seep methane, but observed variability in stable isotope composition and concentration suggest production in two divergent biogeochemical settings that support distinct metabolic pathways of methanogenesis. Comparison of these parameters in raised bogs and seeps indicates that the first is bogs, via CO2 reduction methanogenesis. The second setting is likely groundwater, where dissolved organic carbon from bogs is degraded via chemolithotrophic acetogenesis followed by acetate fermentation methanogenesis. Our findings highlight the importance of methane lateral migration in West Siberia's bog‐dominated landscapes via intimate groundwater connections. The same phenomenon could occur in similar landscapes across the boreal‐taiga biome, thereby making groundwater‐fed rivers and springs potent methane sources.