T‐cell‐dependent antigenic stimulation drives the differentiation of B cells into antibody‐secreting plasma cells and memory B cells, but how B cells regulate this process is unclear. We show that LKB1 expression in B cells maintains B‐cell quiescence and prevents the premature formation of germinal centers (GCs). Lkb1‐deficient B cells (BKO) undergo spontaneous B‐cell activation and secretion of multiple inflammatory cytokines, which leads to splenomegaly caused by an unexpected expansion of T cells. Within this cytokine response, increased IL‐6 production results from heightened activation of NF‐κB, which is suppressed by active LKB1. Secreted IL‐6 drives T‐cell activation and IL‐21 production, promoting T follicular helper (T_FH) cell differentiation and expansion to support a ~100‐fold increase in steady‐state GC B cells. Blockade of IL‐6 secretion by BKO B cells inhibits IL‐21 expression, a known inducer of T_FH‐cell differentiation and expansion. Together, these data reveal cell intrinsic and surprising cell extrinsic roles for LKB1 in B cells that control T_FH‐cell differentiation and GC formation, and place LKB1 as a central regulator of T‐cell‐dependent humoral immunity.