Greenhouse gas (GHG) emissions from abrupt thaw beneath thermokarst lakes were projected to at least double radiative forcing from circumpolar permafrost-soil carbon fluxes by the end of this century, primarily through the release of methane, a much stronger GHG than CO2. Thermokarst lagoons represent the first stage of a thermokarst lake transition to a marine setting with so far neglected consequences for GHG production and release. We expected that along the transition from a thermokarst lake to a thermokarst lagoon, sediment concentrations of terminal electron acceptors like sulfate increase with an associated drop in methanogenic activity, a shift towards non-competitive methylotrophic methanogenesis, and the occurrence of sulfate-driven anaerobic methane oxidation (AOM). To explore this, we targeted a variety of geochemical and microbial parameters including sediment methane and CO2 concentrations, gaseous carbon isotopic signatures, hydrochemistry, GHG production rates, ratios of CH4/CO2, and occurrence of methane-cycling microbial taxa in sediments of two thermokarst lakes and a thermokarst lagoon on the Bykovsky Peninsula located in northeastern Siberia adjacent to Tiksi Bay. We found multiple lines of evidence that AOM in sediment layers influenced by Tiksi Bay water (i.e. the lagoon) functions as effective microbial methane filter. Annually, the lagoon is decoupled from Tiksi Bay for more than six months, resulting in more saline conditions below the ice cover compared to Tiksi Bay. Despite sub-zero near-surface sediment temperatures for approximately nine months per year, we show that, at least in early spring, AOM led to near-surface sediment methane concentrations approximating only about 1% of those measured in near-surface thermokarst lake sediments. Structural equation modelling stresses pore-water chemistry and increases in anaerobic methanotrophic abundance as main controls for the drop of in-situ methane concentrations and the corresponding increase in carbon isotopic signature. Shallow sediment layers (i.e. younger carbon) corresponded with higher rates of potential methane production, especially in the non-lagoon settings but even in the lagoon, potential methane production rates in the surface sediment layers were relatively unaffected by the marine influence. We propose that this reflects the overall dominance of non-competitive methylotrophic methanogenesis independent of pore-water chemistry and sediment depth. Overall, our study suggests that thermokarst lake to lagoon transitions have the potential to offset atmospheric methane fluxes from abrupt thaw lake structures long before thermokarst lakes fully transgress onto the Arctic shelf.