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Methyl mercury, a toxic compound, is produced by anaerobic microbes and magnifies in aquatic food webs, affecting the health of animals and humans. The exploration of mercury methylators based on genomes is still limited, especially in the context of river ecosystems. To address this knowledge gap, we developed a genome catalogue of potential mercury-methylating microorganisms. This was based on the presence of hgcAB from the sediments of a river affected by two run-of-river hydroelectric dams, logging activities and a wildfire. Through the use of genome-resolved metagenomics, we discovered a unique and diverse group of mercury methylators. These were dominated by members of the metabolically versatile Bacteroidota and were particularly rich in microbes that ferment butyrate. By comparing the diversity and abundance of mercury methylators between sites subjected to different disturbances, we found that ongoing disturbances, such as the input of organic matter related to logging activities, were particularly conducive to the establishment of a mercury-methylating niche. Finally, to gain a deeper understanding of the environmental factors that shape the diversity of mercury methylators, we compared the mercury-methylating genome catalogue with the broader microbial community. The results suggest that mercury methylators respond to environmental conditions in a manner similar to the overall microbial community. Therefore, it is crucial to interpret the diversity and abundance of mercury methylators within their specific ecological context.