A co-culture of a novel thermoacidophilic, obligate symbiotic archaeon, designated as strain MJ1^T, with its specific host archaeon Metallosphaera sedula strain MJ1HA was obtained from a terrestrial hot spring in Japan. Strain MJ1^T grew in the co-culture under aerobic conditions. Coccoid cells of strain MJ1^T were 200–500 nm in diameter, and attached to the MJ1HA cells in the co-culture. The ranges and optima of the growth temperature and pH of strain MJ1^T in the co-culture were 60–75 °C (optimum, 65–70 °C) and pH 1.0–4.0 (optimum, pH 2.5), respectively. Core lipids of dialkyl glycerol tetraethers (GDGT)−3 and GDGT-4 were highly abundant in MJ1^T cells concentrated from the co-culture. Strain MJ1^T has a small genome (0.67 Mbp) lacking genes for biosynthesis of essential biomolecules, such as nucleotides, lipids and ATP. The genomic DNA G+C content was 24.9 mol%. The 16S rRNA gene sequence of strain MJ1^T was most closely related to that of the cultivated species, ‘Nanopusillus acidilobi’ strain N7A (85.8 % similarity). Based on phylogenetic and physiological characteristics, we propose the name Nanobdella aerobiophila gen. nov., sp. nov. to accommodate the strain MJ1^T (=JCM 33616^T=DSM 111728^T). In addition, we propose the names Nanobdellaceae fam. nov., Nanobdellales ord. nov., and Nanobdellia class. nov. to accommodate the novel genus.