This study compares predicted sulphur metabolism genes across four Acidihalobacter type strains and two metagenome-assembled genomes (MAGs), revealing genomic differences that appear to correspond to ecological specialization. Phylogenomic analysis separates the species into two clades: clade I includes Acidihalobacter ferrooxydans from a geothermal region in Italy and the two MAGs derived from deep-sea hydrothermal vents in the Pacific Ocean, while clade II comprises Acidihalobacter aeolianus and Acidihalobacter prosperus from a geothermal region in Italy and Acidihalobacter yilgarnensis from a saline and acidic drainage in Australia. Variations in sulphide/quinone oxidoreductases (SQRs) across the species, in particular in Ah. ferrooxydans and Ah. yilgarnensis, likely relate to the availability and speciation of sulphur substrates, which are strictly governed by local redox potential (Eh) and metal redox cycling in their respective habitats. Notably, only Ah. ferrooxydans (clade I) lacks the canonical sulphur/thiosulphate oxidation (Sox) system for thiosulphate oxidation found in clade II and instead encodes components of an alternative S4I pathway. We hypothesize that this difference reflects an adaptation to dynamic microniches going from highly reduced (sulphide-rich) to oxidized metastable sulphur intermediates. In contrast, the retention of the Sox system in clade II suggests a distinct strategy permitting greater metabolic versatility under fluctuating Eh-pH conditions.Differences in clade I terminal oxidases (cbb3-type cytochrome, bc1 complex) and regulatory elements appear to support further adaptation to environments with elevated H2S, setting this clade apart from clade II members. These adaptations, mainly evidenced by gene redundancy, gene loss and horizontal gene transfer, seem to reflect a unique ecological microniche and evolutionary trajectory for Ah. ferrooxydans distinct from other members of the genus, particularly from a sulphur-based energy metabolism perspective.