The precise timing of T cell priming during infection remains unclear. Here, we mapped the cellular dynamics of all immune lineages during acute infection with Listeria monocytogenes (Lm). We identified highly transient activation of conventional type 1 dendritic cells (cDC1s) two days post-infection that functions as a critical time window for priming effector CD8 T cells. Regulation of this transient state was mediated by cDC1-extrinsic IFNγ provided by lymphocytes. Furthermore, antigen-specific T cells that are primed by cDC1s even shortly after this window of peak activation acquire only memory T cell fates. This temporal regulation of fate is recapitulated by cDC1s ex vivo, demonstrating that shifts in activation state of a single antigen presenting cell subset over time regulates CD8 T cell fates. These results uncover a novel mechanism for temporal regulation of CD8 T cell differentiation during a dynamic immune response to acute infection.