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<i>Acidithiobacillus ferridurans</i> JAGS is a newly isolated acidophile from an acid mine drainage (AMD). The genome of isolate JAGS was sequenced and compared with eight other published genomes of <i>Acidithiobacillus</i>. The pairwise mutation distance (Mash) and average nucleotide identity (ANI) revealed that isolate JAGS had a close evolutionary relationship with <i>A. ferridurans</i> JCM18981, but whole-genome alignment showed that it had higher similarity in genomic structure with <i>A. ferrooxidans</i> species. Pan-genome analysis revealed that nine genomes were comprised of 4601 protein coding sequences, of which 43% were core genes (1982) and 23% were unique genes (1064). <i>A. ferridurans</i> species had more unique genes (205–246) than <i>A. ferrooxidans</i> species (21–234). Functional gene categorizations showed that <i>A. ferridurans</i> strains had a higher portion of genes involved in energy production and conversion while <i>A. ferrooxidans</i> had more for inorganic ion transport and metabolism. A high abundance of <i>kdp</i>, <i>mer</i> and <i>ars</i> genes, as well as mobile genetic elements, was found in isolate JAGS, which might contribute to its resistance to harsh environments. These findings expand our understanding of the evolutionary adaptation of <i>Acidithiobacillus</i> and indicate that <i>A. ferridurans</i> JAGS is a promising candidate for biomining and AMD biotreatment applications.