CD8 T cells exhibit dynamic alterations in proliferation and apoptosis during various phases of the CD8 T‐cell response, but the mechanisms that regulate cellular proliferation from the standpoint of CD8 T‐cell memory are not well defined. The cyclin‐dependent kinase inhibitor p27^Kip1 functions as a negative regulator of the cell cycle in T cells, and it has been implicated in regulating cellular processes, including differentiation, transcription and migration. Here, we investigated whether p27^Kip1 regulates CD8 T‐cell memory by T‐cell‐intrinsic or T‐cell‐extrinsic mechanisms, by conditional ablation of p27^Kip1 in T cells or non‐T cells. Studies of T‐cell responses to an acute viral infection show that p27^Kip1 negatively regulates the proliferation of CD8 T cells by T‐cell‐intrinsic mechanisms. However, the enhanced proliferation of CD8 T cells induced by T‐cell‐specific p27^Kip1 deficiency minimally affects the primary expansion or the magnitude of CD8 T‐cell memory. Unexpectedly, p27^Kip1 ablation in non‐T cells markedly augmented the number of high‐quality memory CD8 T cells by enhancing the accumulation of memory precursor effector cells without increasing their proliferation. Further studies show that p27^Kip1 deficiency in immunizing dendritic cells fail to enhance CD8 T‐cell memory. Nevertheless, we have delineated the T‐cell‐intrinsic, anti‐proliferative activities of p27^Kip1 in CD8 T cells from its role as a factor in non‐T cells that restricts the development of CD8 T‐cell memory. These findings have implications in vaccine development and understanding the mechanisms that maintain T‐cell homeostasis.