The establishment of an effective memory T cell population is critical for providing a host with protection from subsequent pathogen re-infection and underpins all effective vaccine strategies. Despite intense study, exactly when memory T cell formation occurs, and the precise factors that drive this process are still be elucidated. To address these questions, we performed extensive single cell RNA-seq (scRNA-seq) on naive, effector (day 3 to 20) and memory influenza A virus (IAV) CD8+ T cells to ask how transcriptional heterogeneity at the single cell level impacts the generation of effective IAV-specific CD8+ T cell immunity. We generated scRNA-seq data and scATAC-seq data from a total of ~36K and 10K cells, respectively. We utilised RNA-velocity analysis to generate cellular trajectories and demonstrated that memory T cell formation is generated in the earliest divisions after T cell activation. Interrogation of transcriptional patterns identified cell division rate as a key factor that determines whether a cell becomes an effector vs memory T cells. To better understand factors that restrain T cell division, we identified key chromatin modifiers appear to regulate early cell division and hence memory T cell differentiation. This approach has the potential to identify novel regulators of the memory state that may be future targets for modulation to promote effective T cell memory.