Aging is associated with a decline in B-lymphopoiesis in the bone marrow and accumulation of long-lived B-cells in the periphery. These changes decrease the body’s ability to mount protective antibody responses. The mechanisms underlining these alterations are poorly understood. We found that the age-related alterations in the B-lineage reflect homeostatic pressures that are imposed by the accumulating long-lived B cells. Thus, a continuous demand for peripheral B cells renders the BM devoid of senescence, and depletion of B cells in old mice revives B cell production in the bone marrow and rejuvenates the peripheral B cell compartment. Collectively, our studies suggest that immunosenescence in the B-lineage can be reversed to enhance immune responsiveness in aging.