T follicular helper (Tfh) cells provide essential survival and selection signals to germinal center (GC) B cells that are important for protective and long-lived antibody responses. It has become clear that tight control of Tfh cell numbers is important to impose competition amongst B cells in the germinal centers and set a selection threshold that will favour survival of high affinity clones. Although multiple signals are now known to be required for Tfh cell formation, surprisingly little is known about the mechanisms that limit Tfh cell numbers. Here we show that miR-146a, a microRNA frequently dysregulated in systemic autoimmunity, is highly expressed in Tfh cells and its peak expression during a T-dependent immune response marks the decline of the Tfh cell population. Loss of miR-146a caused cell-autonomous accumulation of Tfh and GC B cells. MiR-146a directly repressed several Tfh-expressed mRNAs including Icos, Slamf1, Slamf6, Cd84, Stat1, Notch1 and Cxcr4. Of these, ICOS was the most strongly and cell-intrinsically upregulated target in miR-146a-deficient T cells. Partial blockade of ICOS signaling, either by injections of sub-optimal dose of blocking antibody or by halving the gene dose of Icos in miR-146a-deficient Tfh cell precursors, prevented the Tfh and GC B cell accumulation. Additional factors including STAT1 overexpression in T cells, mildly enhanced T-cell sensitivity to IL-6 signaling, and increased ICOS ligand expression on GC B cells and other antigen-presenting cells, might collectively act to exacerbate the expansion of Tfh and GC B cells in miR-146a-deficient mice. Thus miR-146a emerges as a post-transcriptional brake to limit the magnitude of GC responses.