<p>Toxic methylmercury (CH₃Hg⁺) is produced by microbial conversion of inorganic mercury in hypoxic environments such as rice paddy soils, and can accumulate in rice grains. Although microbial demethylation has been recognized as a crucial pathway for CH₃Hg⁺ degradation, the identities of microbes and pathways accountable for CH₃Hg⁺ degradation in soil remain elusive. Here, we combine ¹³CH₃Hg⁺-DNA stable-isotope probing experiments with shotgun metagenomics to explore microbial taxa and associated biochemical processes involved in CH₃Hg⁺ degradation in paddy and upland soils. We identify <i>Pseudarthrobacter</i>, <i>Methylophilaceae</i> (MM2), and <i>Dechloromonas</i> as the most significant taxa potentially engaged in the degradation of ¹³CH₃Hg⁺ in paddy soil with high mercury contamination. We confirm that strains affiliated with two of those taxa (species <i>Dechloromonas denitrificans</i> and <i>Methylovorus menthalis</i>) can degrade CH₃Hg⁺ in pure culture assays. Metagenomic analysis further reveals that most of these candidate ¹³CH₃Hg⁺ degraders carry genes associated with the Wood-Ljungdahl pathway, dicarboxylate-hydroxybutyrate cycle, methanogenesis, and denitrification, but apparently lack the <i>merB</i> and <i>merA</i> genes involved in CH₃Hg⁺ reductive demethylation. Finally, we estimate that microbial degradation of soil CH₃Hg⁺ contributes to 0.08–0.64 fold decreases in CH₃Hg⁺ accumulation in rice grains across China (hazard quotient (HQ) decrements of 0.62–13.75%). Thus, our results provide insights into microorganisms and pathways responsible for CH₃Hg⁺ degradation in soil, with potential implications for development of bioremediation strategies.</p>