Recent omics studies have provided invaluable insights into the metabolic potential, adaptation, and evolution of novel archaeal lineages from a variety of extreme environments. We utilized a genome-resolved metagenomic approach to recover eight medium- to high-quality metagenome-assembled genomes (MAGs) that likely represent a new order (" Sysuiplasmatales") in the class from mine tailings and acid mine drainage (AMD) sediments sampled from two copper mines in South China. 16S rRNA gene-based analyses revealed a narrow habitat range for these uncultured archaea limited to AMD and hot spring-related environments. Metabolic reconstruction indicated a facultatively anaerobic heterotrophic lifestyle. This may allow the archaea to adapt to oxygen fluctuations and is thus in marked contrast to the majority of lineages in the domain , which typically show obligately anaerobic metabolisms. Notably, " Sysuiplasmatales" could conserve energy through degradation of fatty acids, amino acid metabolism, and oxidation of reduced inorganic sulfur compounds (RISCs), suggesting that they may contribute to acid generation in the extreme mine environments. Unlike the closely related orders and " Gimiplasmatales," " Sysuiplasmatales" lacks the capacity to perform methanogenesis and carbon fixation. Ancestral state reconstruction indicated that " Sysuiplasmatales," the closely related orders and " Gimiplasmatales," and the orders SG8-5 and RBG-16-68-12 originated from a facultatively anaerobic ancestor capable of carbon fixation via the bacterial-type HF Wood-Ljungdahl pathway (WLP). Their metabolic divergence might be attributed to different evolutionary paths. A wide array of archaea populate Earth's extreme environments; therefore, they may play important roles in mediating biogeochemical processes such as iron and sulfur cycling. However, our knowledge of archaeal biology and evolution is still limited, since the majority of the archaeal diversity is uncultured. For instance, most order-level lineages except , , and within do not have cultured representatives. Here, we report the discovery and genomic characterization of a novel order, ". Sysuiplasmatales," within in extremely acidic mine environments. ". Sysuiplasmatales" are inferred to be facultatively anaerobic heterotrophs and likely contribute to acid generation through the oxidation of RISCs. The physiological divergence between ". Sysuiplasmatales" and closely related lineages may be attributed to different evolutionary paths. These results expand our knowledge of archaea in the extreme mine ecosystem.