The CXC chemokine receptor (CXCR)5 is rapidly induced on activated CD4(+) T cells, allowing migration toward secondary lymphoid tissue follicles, where the CXCR5 ligand CXCL13/BCA-1 is produced. Such CXCR5(+) T cells provide efficient help for B cell immunoglobulin production and are termed follicular B helper T (T(FH)) cells. However, the molecular mechanisms by which T(FH) cells provide B cell help are unknown. Here, we demonstrate that newly generated (antigen-primed) T(FH) cells express a phenotype consistent with induction of B cell proliferation, but co-culture with primed B cells resulted in a switch to a plasma cell-inducing phenotype, characterized by loss of CD154, induction of CD70 and an increase in IL-10 production capacity. The ability to produce IL-10 could be maintained as a stable phenotype, but its secretion was strictly dependent on inducible costimulator (ICOS) signaling. Furthermore, B cells preserved a lymph node migration phenotype in proliferating T(FH) cells by preventing the loss of CC chemokine receptor (CCR)7 and the induction of CCR5. Thus, B cells directly modulate the B cell helper phenotype in T(FH) cells and actively promote their prolonged co-localization with these cells.