High-affinity B cell selection in the germinal center (GC) is governed by signals delivered by follicular helper T (Tfh) cells to B cells. Selected B cells undergo clonal expansion and affinity maturation in the GC dark zone in direct proportion to the amount of antigen they capture and present to Tfh cells in the light zone. Here, we examined the mechanisms whereby Tfh cells program the number of GC B cell divisions. Gene expression analysis revealed that Tfh cells induce Myc expression in light-zone B cells in direct proportion to antigen capture. Conditional Myc haplo-insufficiency or overexpression combined with cell division tracking showed that MYC expression produces a metabolic reservoir in selected light-zone B cells that is proportional to the number of cell divisions in the dark zone. Thus, MYC constitutes the GC B cell division timer that when deregulated leads to emergence of B cell lymphoma. Display omitted •MYC expression in light-zone B cells is proportional to the magnitude of T cell help•MYC proportionally regulates the size of light-zone germinal center B cells•MYC amounts dictate division capacity and residence time in the dark zone B cell clonal expansion is regulated by Tfh cells in the germinal center. Finkin et al. report that Tfh cells induce Myc expression by light-zone B cells in direct proportion to the amount of antigen presented, and that MYC proportionally regulates B cell size and division in the dark zone.