Methanotrophs play a crucial role in mitigating methane (CH4) emission by oxidizing produced CH4 in paddy soils; however, ecological drivers of methanotrophic community in the soils around heavy metal contaminated areas remain unclear. In this study, we evaluated the effects of heavy metal pollution and soil properties on the abundance, diversity and composition of methanotrophic community in paddy soils from two typical mercury (Hg) mining regions in southwest China. The results of random forest and structure equation models suggest that both heavy metal content and soil nutrients greatly influenced the attributes of methanotrophic community. In general, the abundance and diversity of methanotrophs were negatively related to soil Hg content, but showed positive correlation with soil organic carbon content. However, the other metals (cadmium (Cd), nickel (Ni), lead (Pb), arsenic (As), zinc (Zn)) had inconsistent associations with the microbial indexes of methanotrophic community in the soil. Elevated levels of heavy metal and nutrients in the soils shifted the community composition of methanotrophs. For example, Pb, As and Zn contents had negative associations with the relative abundance of Methylocaldum. In addition, changes in the relative abundance of ecological clusters within the co-occurrence network of methanotrophs were related to metal contents and soil properties. Together, our findings provide novel insights into understanding ecological drivers of methanotrophic community in paddy soils around Hg mining regions, with important implications for mitigating CH4 emissions in terrestrial ecosystems.