The candidate phylum T1-SED10-126 is known from hypersaline and alkaline settings, but its genomic potential remains poorly understood. This study uses genome-resolved metagenomics and pangenomic analysis to characterise the metabolic, physiological, and evolutionary features of this phylum. Analysis of > 200 global metagenomes confirmed T1-SED10-126 is widespread but rare (< 2 % abundance), exclusively inhabiting high-salinity and/or high-alkalinity environments. Further metagenomic analysis identified 12 Metagenome-Assembled Genomes (MAGs) belonging to T1-SED10-126, including three novel MAGs recovered from hypersaline environments. Average Nucleotide and Amino Acid Identity comparisons of the 12 MAGs revealed high internal genetic diversity, forming at least two distinct phylogenetic clusters that likely represent novel families or genera. All MAGs are predicted halophiles, but physiological modelling identified a clear functional divergence, with one clade predicted to be alkaliphilic and anaerobic, while the other is neutrophilic and aerotolerant. This split is mirrored in their core metabolic pathways (e.g., ATPase type, carboxydotrophy vs. aerobic respiration) and adaptations to nutrient scarcity. Analysis of the mobilome revealed a dynamic genomic architecture, characterised by independently acquired CRISPR-Cas systems and a high abundance of insertion sequence (IS) elements. This pangenomic analysis of T1-SED10-126 illuminates the ecological strategies of a deeply branching extremophilic phylum, highlighting distinct evolutionary trajectories driven by a highly plastic genome.