Advances in genetics have allowed for greater investigation into the complex microbial communities mediating mercury methylation in the environment. In wetlands in particular, dissolved organic matter (DOM) may influence methylmercury production both through direct chemical interactions with mercury and through substrate effects on the environmental microbiome. We conducted microcosm experiments in two chemically disparate wetland environments (unvegetated and vegetated sediments) to examine the impact of DOM from leachate of local vegetation and inorganic mercury loadings on microbial community membership, metagenomic potential, DOM processing, and methylmercury production. We show that while DOM loadings impacted the microbiome in both environment types, sediment with high organic carbon content was more resistant than oligotrophic sediment to changes in microbial community structure and methylmercury production. We identify putative chemoorganotrophic methylators within the class Clostridia as primary community members associated with methylation rates in contrast to previous work focusing on microorganisms involved in sulfur, iron, and methane cycling. Metagenomic shifts toward fermentation, and secondarily iron metabolisms, as well as degradation of complex DOM indicated by fluorescence indices further support the involvement of rarely acknowledged biogeochemical pathways in mercury toxicity. We therefore propose that DOM addition in our system generates methylmercury production either 1) via direct methylation by fermenting bacteria or 2) via enhancing the bioavailability of simple carbon compounds for sulfate- and iron-reducing bacteria through breakdown of complex DOM. Our results demonstrate variation in sediment methylmercury production in response to DOM loading across geochemical environments and provide a mechanistic framework for understanding linkages between environmental microbiomes, carbon cycling, and mercury toxicity.