This study investigates the extracellular electron transfer (EET) mechanisms of anaerobic methanotrophic archaea (ANME-2d, *Ca. Methanoperedens*). ANME-2d are environmentally significant microorganisms that oxidize methane, a potent greenhouse gas. The research team cultivated *Ca. Methanoperedens* in bioelectrochemical systems and observed a strong methane-dependent current (91-93% of total current) associated with high enrichment of *Ca. Methanoperedens* on the anode (up to 82% of the community). Electrochemical and metatranscriptomic analyses suggested that the EET mechanism remains similar at various electrode potentials, involving an uncharacterized short-range electron transport protein complex and OmcZ nanowires. The study conducted three experiments to investigate EET by *Ca. Methanoperedens* using bioelectrochemical systems at different anode potentials. The results showed that the methane-dependent current was not affected by the applied potential, and the microbial community consumed an average of 71 ± 0.017 μmol methane day^-1^. Confocal laser scanning microscopy, scanning electron microscopy, and transmission electron microscopy revealed spatial organization of the biofilm microbial community, with *Ca. Methanoperedens* forming large aggregates and associated bacteria, particularly *Geobacter*, being present near the gold mesh. Metagenomic and metatranscriptomic analyses identified two gene clusters likely involved in EET: one encoding multiple multi-heme c-type cytochromes (MHCs) and another encoding proteins homologous to OmcZ nanowires. These gene clusters were upregulated under electrogenic growth conditions compared to nitrate-dependent growth. The study also found that antibiotics targeting bacteria did not affect the methane-dependent current, suggesting a low contribution of bacteria to the total current produced. In conclusion, the research provides evidence for current production and EET by *Ca. Methanoperedens* during methane oxidation, either through direct interspecies electron transfer with *Geobacter* or independently, possibly via cytochrome-containing nanowires. These findings have implications for anaerobic methanotrophs in the environment and offer opportunities for sustainable biotechnological applications.This study investigates the extracellular electron transfer (EET) mechanisms of anaerobic methanotrophic archaea (ANME-2d, *Ca. Methanoperedens*). ANME-2d are environmentally significant microorganisms that oxidize methane, a potent greenhouse gas. The research team cultivated *Ca. Methanoperedens* in bioelectrochemical systems and observed a strong methane-dependent current (91-93% of total current) associated with high enrichment of *Ca. Methanoperedens* on the anode (up to 82% of the community). Electrochemical and metatranscriptomic analyses suggested that the EET mechanism remains similar at various electrode potentials, involving an uncharacterized short-range electron transport protein complex and OmcZ nanowires. The study conducted three experiments to investigate EET by *Ca. Methanoperedens* using bioelectrochemical systems at different anode potentials. The results showed that the methane-dependent current was not affected by the applied potential, and the microbial community consumed an average of 71 ± 0.017 μmol methane day^-1^. Confocal laser scanning microscopy, scanning electron microscopy, and transmission electron microscopy revealed spatial organization of the biofilm microbial community, with *Ca. Methanoperedens* forming large aggregates and associated bacteria, particularly *Geobacter*, being present near the gold mesh. Metagenomic and metatranscriptomic analyses identified two gene clusters likely involved in EET: one encoding multiple multi-heme c-type cytochromes (MHCs) and another encoding proteins homologous to OmcZ nanowires. These gene clusters were upregulated under electrogenic growth conditions compared to nitrate-dependent growth. The study also found that antibiotics targeting bacteria did not affect the methane-dependent current, suggesting a low contribution of bacteria to the total current produced. In conclusion, the research provides evidence for current production and EET by *Ca. Methanoperedens* during methane oxidation, either through direct interspecies electron transfer with *Geobacter* or independently, possibly via cytochrome-containing nanowires. These findings have implications for anaerobic methanotrophs in the environment and offer opportunities for sustainable biotechnological applications.