<p>The Cuatro Cienegas Basin (CCB) in Mexico, represents a unique ecological habitat, characterized by extreme and fluctuating conditions, providing a window into ancient evolutionary processes. This basin, characterized by hypersalinity and phosphorus scarcity, harbors diverse microbial communities that exhibit remarkable adaptations to oligotrophic conditions. Among these, <i>Halobacterium salinarum</i>, a halophilic archaeon known for its polyploid genome and metabolic versatility, has been extensively studied as a model for extremophile survival. However, only a limited number of <i>H. salinarum</i> strains have been successfully cultured and characterized to date. Here, we report the isolation and genomic analysis of a novel <i>Halobacterium salinarum</i> strain, AD88, from microbial mats at the Archaean Domes site in the CCB. This strain displays unique genomic features, including smaller plasmid sizes and distinctive metabolic pathways for phosphorus and sulfur utilization. Comparative analyses with other <i>Halobacterium</i> strains revealed genetic innovations, such as genes involved in sulfolipid biosynthesis, enabling membrane stability in phosphorus-depleted environments, and adaptations for horizontal gene transfer, which facilitate genomic flexibility in response to environmental pressures. This study reveals that <i>H. salinarum</i> AD88 is the first recorded diploid strain of <i>Halobacterium</i>, a feature previously undocumented in this genus. Phylogenomic reconstruction positioned AD88 tightly within the <i>Halobacterium</i> clade, reflecting its evolutionary history within the genus. Pangenome analysis further highlighted the open nature of the <i>Halobacterium</i> genus, with AD88 contributing novel accessory genes linked to ecological specialization. These findings emphasize the evolutionary significance of the CCB as a natural laboratory for studying microbial adaptation and expand our understanding of archaeal genomic diversity and functional innovation under extreme conditions.</p>