Summary Anaerobic oxidation of methane greatly contributes to global carbon cycling, yet the anaerobic oxidation of non‐methane alkanes by archaea was only recently detected in lab enrichments. The distribution and activity of these archaea in natural environments are not yet reported and understood. Here, a combination of metagenomic and metatranscriptomic approaches was utilized to understand the ecological roles and metabolic potentials of methyl‐coenzyme M reductase (MCR)‐based alkane oxidizing (MAO) archaea in Guaymas Basin sediments. Diverse MAO archaea, including multi‐carbon alkane oxidizer Ca . Syntrophoarchaeum spp., anaerobic methane oxidizing archaea ANME‐1 and ANME‐2c as well as sulfate‐reducing bacteria HotSeep‐1 and Seep‐SRB2 that potentially involved in MAO processes, coexisted and showed activity in Guaymas Basin sediments. High‐quality genomic bins of Ca . Syntrophoarchaeum spp., ANME‐1 and ANME‐2c were retrieved. They all contain and expressed mcr genes and genes in Wood–Ljungdahl pathway for the complete oxidation from alkane to CO 2 in local environment, while Ca . Syntrophoarchaeum spp. also possess beta‐oxidation genes for multi‐carbon alkane degradation. A global survey of potential multi‐carbon alkane metabolism archaea shows that they are usually present in organic rich environments but are not limit to hydrothermal or marine ecosystems. Our study provided new insights into ecological and metabolic potentials of MAO archaea in natural environments.