Members of the class Campylobacteria are microaerophilic bacteria widely distributed across diverse environments and are abundant in hydrothermal systems. However, cultivated representatives, particularly from shallow-water vents, remain limited. Here, we investigated the genomic diversity and environmental adaptation of the genus Sulfurospirillum. Phylogenomic analysis revealed a clear separation between terrestrial and marine clades, with relatively few cultured representatives in the marine lineage. Strain 1307, isolated from shallow-water hydrothermal vents, expands the genomic representation of this underexplored clade. Pan-genome analyses based on complete genomes revealed an open pan-genome, indicating ongoing diversification of genus Sulfurospirillum. Further comparison between hydrothermal vent (HTV) and non-HTV lineages identified distinct adaptive features. Vent-associated strains are enriched in genes involved in sulfur metabolism, carbon fixation, the glycine cleavage system (GCS), and the biosynthesis of key cofactors (spermidine, thiamine, lipoate, and heme), reflecting metabolic adaptation to hydrothermal environments. Beyond well-established processes such as sulfur metabolism and autotrophic carbon fixation, the widespread presence of the GCS in vent-associated lineages suggests its potential role as an auxiliary carbon fixation pathway under anaerobic conditions. Overall, this study expands the phylogenetic and genomic diversity of Sulfurospirillum and offers new insights into the mechanisms underlying environmental adaptation and niche differentiation in vent-associated Campylobacteria.