Abstract Naive antigen-specific CD8 T cells expand in response to infection and can be phenotypically separated into distinct effector populations, which include memory precursor effector cells and short-lived effector cells. In the days before the peak of the T cell response, a third population called early effector cells (EECs) predominate the antigen-specific response. However, the contribution of the EEC population to the CD8 T cell differentiation program during an immune response is not well understood. Here we show that EECs were pre-programmed to differentiate based on early signals received from distinct infectious environments, but surprisingly, when these same EECs were transferred into infected hosts, the EECs could be diverted from their original fate by a disparate inflammatory environment. After observing plasticity at the population level, we also examined the antiviral and antibacterial responses of single CD8 T cells from the polyclonal repertoire. The progeny of naive clonal CD8 T cells displayed unique profiles of differentiation based on extrinsic pathogen-induced environmental cues, with some clones demonstrating extreme bias toward a single developmental pathway. These results, taken together, demonstrate that stochastic and instructive events differentially contribute to shaping the CD8 T cell response and provide insight into the underlying forces that drive effector differentiation and protective memory formation.