The concept is emerging that the bone marrow (BM) sustains life-long persistence of memory T cells, as it does for plasma cells. Recent studies revived the debate on how this is achieved: is the BM essentially a nest for the proliferation of recirculating memory T cells, or a storage depot for resting memory T cells? Learning from division of labor in hematopoietic stem cells, this article proposes that two distinct BM niches support memory T cell cycling and quiescence, thereby enabling memory T cells to maintain all their distinguishing features. This framework might be instrumental to interpret some puzzling findings and conceptualize the mechanisms preserving either stability of memory T cell numbers or the capacity to mount secondary responses.