IL-15 regulates central and effector memory CD8 T cell (T CM and T EM, respectively) homeostatic proliferation, maintenance, and longevity. Consequently, IL-15 availability hypothetically defines the carrying capacity for total memory CD8 T cells within the host. In conflict with this hypothesis, previous observations demonstrated that boosting generates preternaturally abundant T EM that increases the total quantity of memory CD8 T cells in mice. In this article, we provide a potential mechanistic explanation by reporting that boosted circulating T EM do not require IL-15 for maintenance. We also investigated tissue-resident memory CD8 T cells (T RM), which protect nonlymphoid tissues from reinfection. We observed up to a 50-fold increase in the total magnitude of T RM in mouse mucosal tissues after boosting, suggesting that the memory T cell capacity in tissues is flexible and that T RM may not be under the same homeostatic regulation as primary central memory CD8 T cells and T EM. Further analysis identified distinct T RM populations that depended on IL-15 for homeostatic proliferation and survival, depended on IL-15 for homeostatic proliferation but not for survival, or did not depend on IL-15 for either process. These observations on the numerical regulation of T cell memory indicate that there may be significant heterogeneity among distinct T RM populations and also argue against the common perception that developing vaccines that confer protection by establishing abundant T EM and T RM will necessarily erode immunity to previously encountered pathogens as the result of competition for IL-15.