Production of high-affinity antibody responses after infection or vaccination requires precise control of germinal center B cells by follicular helper T cells and follicular regulatory T cells. Although the Bcl6 transcription factor plays a central role in follicular T cell differentiation, the molecular basis of Bcl6 control has been clouded in uncertainty. Here we report that Bcl6-dependent control reflects the formation of a macromolecular complex between Bcl6 and the Mi-2β-nucleosome remodeling deacetylase complex (Mi-2β-NuRD). The repressive activity of this intranuclear complex potentiates the follicular T cell phenotype and inhibits alternative T cell fates. Identification of this intracellular complex may facilitate new targeted approaches to the treatment of autoimmune disorders.