Cadmium (Cd), chromium (Cr) and lead (Pb) are heavy metals that have been classified as priority pollutants in aqueous environment while methane-oxidizing bacteria as a biofilter arguably consume up to 90% of the produced methane in the same aqueous environment before it escapes into the atmosphere. However, the underlying kinetics and active methane oxidizers are poorly understood for the hotspot of epipelon that provides a unique micro-ecosystem containing diversified guild of microorganisms including methane oxidizers for potential bioremediation of heavy metals. In the present study, the Pb2+, Cd2+and Cr6+ bioremediation potential of epipelon biofilm was assessed under both high (120,000 ppm) and near-atmospheric (6 ppm) methane concentrations. Epipelon biofilm demonstrated a high methane oxidation activity following microcosm incubation amended with a high concentration of methane, accompanied by the complete removal of 50 mg L−1 Pb2+ and 50 mg L−1 Cd2+ (14 days) and partial (20%) removal of 50 mg L−1 Cr6+ after 20 days. High methane dose stimulated a faster (144 h earlier) heavy metal removal rate compared to near-atmospheric methane concentrations. DNA-based stable isotope probing (DNA-SIP) following13CH4 microcosm incubation revealed the growth and activity of different phylotypes of methanotrophs during the methane oxidation and heavy metal removal process. High throughput sequencing of13C-labelled particulate methane monooxygenase gene pmoA and 16S rRNA genes revealed that the prevalent active methane oxidizers were type I affiliated methanotrophs, i.e., Methylobacter. Type II methanotrophs including Methylosinus and Methylocystis were also labeled only under high methane concentrations. These results suggest that epipelon biofilm can serve as an important micro-environment to alleviate both methane emission and the heavy metal contamination in aqueous ecosystems with constant high methane fluxes.