Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial populations, we examined 22 metagenome-assembled genomes (MAGs) (70 to 97% complete) from the ubiquitous vent Epsilonbacteraeota genus Sulfurovum that were recovered from two deep-sea hydrothermal vent regions, Axial Seamount in the northeastern Pacific Ocean (13 MAGs) and the Mid-Cayman Rise in the Caribbean Sea (9 MAGs). Genes involved in housekeeping functions were highly conserved across Sulfurovum lineages. However, genes involved in environment-specific functions, and in particular phosphate regulation, were found mostly in Sulfurovum genomes from the Mid-Cayman Rise in the low-phosphate Atlantic Ocean environment, suggesting that nutrient limitation is an important selective pressure for these bacteria. Furthermore, genes that were rare within the pangenome were more likely to undergo positive selection than genes that were highly conserved in the pangenome, and they also appeared to have experienced gene-specific sweeps. Our results suggest that selection is a significant driver of gene gain and loss for dominant microbial lineages in hydrothermal vents and highlight the importance of factors like nutrient limitation in driving microbial adaptation and evolution.