Regulatory T cells (T) accumulate in the visceral adipose tissue (VAT) to maintain systemic metabolic homeostasis but decline during obesity. Here, we explored the metabolic pathways controlling the homeostasis, composition, and function of VAT T under normal and high-fat diet feeding conditions. We found that cholesterol metabolism was specifically up-regulated in ST2 VAT T subsets. T-specific deletion of , the master regulator of cholesterol homeostasis, selectively reduced ST2 VAT T, increasing VAT inflammation and insulin resistance. Single-cell RNA/T cell receptor (TCR) sequencing revealed a specific loss and reduced clonal expansion of ST2 VAT T subsets after deletion. -mediated cholesterol homeostasis potentiated strong TCR signaling, which preferentially promoted ST2 VAT T accumulation. However, long-term high-fat diet feeding disrupted VAT T cholesterol homeostasis and impaired clonal expansion of the ST2 subset. Restoring T cholesterol homeostasis rescued VAT T accumulation in obese mice, suggesting that modulation of cholesterol homeostasis could be a promising strategy for T-targeted therapies in obesity-associated metabolic diseases.