The distribution of Archaea and methanogenic, methanotrophic and sulfate-reducing communities in three Atlantic ultramafic-hosted hydrothermal systems (Rainbow, Ashadze, Lost City) was compared using 16S rRNA gene and functional gene (mcrA, pmoA and dsrA) clone libraries. The overall archaeal community was diverse and heterogeneously distributed between the hydrothermal sites and the types of samples analyzed (seawater, hydrothermal fluid, chimney and sediment). The Lost City hydrothermal field, characterized by high alkaline warm fluids (pH>11; T<95 °C), harbored a singular archaeal diversity mostly composed of unaffiliated Methanosarcinales. The archaeal communities associated with the recently discovered Ashadze 1 site, one of the deepest active hydrothermal fields known (4100 m depth), showed significant differences between the two different vents analyzed and were characterized by putative extreme halophiles. Sequences related to the rarely detected Nanoarchaeota phylum and Methanopyrales order were also retrieved from the Rainbow and Ashadze hydrothermal fluids. However, the methanogenic Methanococcales was the most widely distributed hyper/thermophilic archaeal group among the hot and acidic ultramafic-hosted hydrothermal system environments. Most of the lineages detected are linked to methane and hydrogen cycling, suggesting that in ultramafic-hosted hydrothermal systems, large methanogenic and methanotrophic communities could be fuelled by hydrothermal fluids highly enriched in methane and hydrogen.