This study investigates the mechanisms of extracellular electron transfer (EET) in anaerobic methanotrophic archaea, specifically 'Ca. Methanoperedens', using bioelectrochemical systems. The research demonstrates that 'Ca. Methanoperedens' can transfer electrons to an electrode across a range of potentials (0–600 mV vs SHE), with a strong methane-dependent current (91–93% of total current) observed. Metagenomic and metatranscriptomic analyses reveal that the EET mechanism is consistent across different electrode potentials, involving an uncharacterized short-range electron transport protein complex and OmcZ nanowires. The study also shows that 'Ca. Methanoperedens' can dominate microbial communities on the anode, reaching up to 82% abundance. The research highlights that 'Ca. Methanoperedens' expresses genes for proteins with structural similarities to OmcZ nanowires in Geobacter sulfurreducens, suggesting a potential role in long-range electron transfer. Additionally, the study identifies two gene clusters likely involved in EET, including multiple multi-heme c-type cytochromes (MHCs). These findings suggest that 'Ca. Methanoperedens' may use diverse extracellular electron acceptors without altering its EET mechanism, unlike Geobacter, which can adapt its EET strategy to different redox potentials. The study also shows that the expression of EET-related genes is not significantly affected by changes in electrode potential, indicating that 'Ca. Methanoperedens' may not need to adjust its expression pattern for different electron acceptors. The results suggest that 'Ca. Methanoperedens' can perform electrogenic anaerobic oxidation of methane independently of syntrophic partners, which has implications for understanding the role of anaerobic methanotrophs in the environment and their potential applications in biotechnology. The study provides evidence for current production and extracellular electron transfer by 'Ca. Methanoperedens' during methane oxidation, either through direct interspecies electron transfer with Geobacter or via cytochrome-containing nanowires. These findings have significant implications for climate change and sustainable biotechnological applications.This study investigates the mechanisms of extracellular electron transfer (EET) in anaerobic methanotrophic archaea, specifically 'Ca. Methanoperedens', using bioelectrochemical systems. The research demonstrates that 'Ca. Methanoperedens' can transfer electrons to an electrode across a range of potentials (0–600 mV vs SHE), with a strong methane-dependent current (91–93% of total current) observed. Metagenomic and metatranscriptomic analyses reveal that the EET mechanism is consistent across different electrode potentials, involving an uncharacterized short-range electron transport protein complex and OmcZ nanowires. The study also shows that 'Ca. Methanoperedens' can dominate microbial communities on the anode, reaching up to 82% abundance. The research highlights that 'Ca. Methanoperedens' expresses genes for proteins with structural similarities to OmcZ nanowires in Geobacter sulfurreducens, suggesting a potential role in long-range electron transfer. Additionally, the study identifies two gene clusters likely involved in EET, including multiple multi-heme c-type cytochromes (MHCs). These findings suggest that 'Ca. Methanoperedens' may use diverse extracellular electron acceptors without altering its EET mechanism, unlike Geobacter, which can adapt its EET strategy to different redox potentials. The study also shows that the expression of EET-related genes is not significantly affected by changes in electrode potential, indicating that 'Ca. Methanoperedens' may not need to adjust its expression pattern for different electron acceptors. The results suggest that 'Ca. Methanoperedens' can perform electrogenic anaerobic oxidation of methane independently of syntrophic partners, which has implications for understanding the role of anaerobic methanotrophs in the environment and their potential applications in biotechnology. The study provides evidence for current production and extracellular electron transfer by 'Ca. Methanoperedens' during methane oxidation, either through direct interspecies electron transfer with Geobacter or via cytochrome-containing nanowires. These findings have significant implications for climate change and sustainable biotechnological applications.