Obesity is an inflammatory disease that leads to chronic, low-grade inflammation in adipose tissue which contributes to the development of type 2 diabetes (T2D). Adipose tissue-resident immune cells maintain homeostasis in lean patients and regulate or exacerbate inflammation in obese patients. Understanding the role of these immune cells will be critical for treating metabolic disease. iNKT cells and cytokine-producing B cells are enriched in white adipose tissue as compared with spleen, and these populations change during obesity. We determined that cytokine-producing B cells in adipose tissue share phenotypic traits with memory- or alternatively activated B cells, including T–bet and CD11c expression. We find that these and other B cells in VAT are supported by iNKT cells in both lean and obese states. Specifically, obese mice showed a significant drop in their frequency of IL-10⁺ adipose B cells and a concomitant increase in frequency of Tbet⁺CD11c⁺CD11b⁺ adipose B cells, as compared to lean mice. We find the same pattern of B cell activation and a decrease in IL-10⁺ B cells in human adipose tissue from overweight/obese patients as compared to lean patients. We also find that glycolipid activation of iNKT cells skews adipose tissue B cells to produce anti-inflammatory cytokines, suggesting iNKT activation may provide a therapeutic approach to restore regulatory B cell homeostasis in adipose tissue of obese subjects and reduce metabolic symptoms associated with T2D.