CD8+ T cells are key adaptive immune cells that are pivotal for control of virus infections and tumour surveillance. Upon activation, CD8+ T cells undergo a program of differentiation and proliferations whereby they acquire lineage specific functions that underpin their role in immunity. The strict control of gene expression driving CD8+ T cell differentiation is underpinned by spatial and temporal changes in chromatin biochemical modifications such as histone H3 lysine modifications. However, unlike lysine modifications, the role of histone arginine modifications in T cell differentiation is a neglected area. In this study, we demonstrate that the activation of naïve CD8+ T cell results in the upregulation of PRMT1 and PRMT5, the protein arginine (R) methyltransferases responsible for the asymmetric and symmetric dimethylation (me2) of histone H2A (H2AR3me2) and histone H4 (H4R3me2), respectively. This upregulation is correlated with temporal increase in the level of R3me2 in activated T cells. Besides, CRISPR depletion of PRMTs results in impaired effector expansion after T cell activation, while PRMT5 knockout leads to a higher retention of memory cells. Furthermore, our Cut&Tag and RNA-seq analyses reveal that PRMTs are essential for TCF1/β-catenin signalling and metabolic processes. These findings suggest that the dynamic regulation of histone arginine methylation by PRMTs plays a crucial role in shaping chromatin structures that support optimal CD8+ T cell fate decisions, highlighting a potential new strategy for enhancing immunotherapies.