Billions of tons of dimethylsulfoniopropionate (DMSP) are produced annually in coastal ecosystems, yet its fate in anaerobic sediments remains underexplored. Here, we combined stable-isotope probing (DNA-SIP) with 16S rRNA amplicon sequencing to pinpoint microorganisms actively degrading DMSP in anoxic Blakeney salt-marsh sediments and to track volatile sulfur and methane formation. Anaerobic microcosms (4 g sediment/40 ml seawater) were amended with ¹³C- or ¹²C-DMSP (100–200 μM). DMSP was rapidly depleted (≤24 h to <10%), coincident with stoichiometric, sustained DMS accumulation and transient MeSH, while autoclaved controls showed no change. Methane increased throughout incubations, indicating a previously overlooked conduit from DMSP-derived carbon to methanogenesis under anoxic conditions. After assimilation (up to 800 h), isopycnic ultracentrifugation resolved heavy ¹³C-DNA. 16S profiles revealed pronounced enrichment of Dethiosulfatibacter (Clostridia) together with methylotrophic Methanolobus and Bathyarchaeia in ¹³C-heavy fractions relative to ¹³C-light and ¹²C controls, identifying these anaerobic lineages as the principal DMSP carbon assimilators. In contrast, light fractions were richer in sulfur-oxidising and sulfate-reducing taxa that did not incorporate labels, consistent with secondary metabolism and cross-feeding. Culture-dependent work recovered diverse Alpha- and Gammaproteobacteria able to use DMSP, typically producing DMS but rarely MeSH, supporting a dominant lyase-type route under these conditions. Our results show significant DMSP pools in anoxic salt-marsh sediments and reveal the active DMSP degraders and link to methane formation under anaerobic conditions.