During hematopoiesis the equilibrium that is established between the many diverse immune cell populations is essential for defense against invasion by foreign pathogens. Thus, it is critical to understand how this process is regulated as disruptions to this delicate cellular balance can have dramatic consequences such autoimmune disease. We have found that the specific ablation of a histone methyltransferase (HMTase) in the T cell lineage results in perturbation to immune homeostasis due to the aberrant accumulation of an innate T cell population that induces CD8 T cells to spontaneously adopt a memory-like phenotype. Surprisingly, in this context the HMTase appears to act independently of its traditional role as a histone methyltransferase. We found that HMTase directly methylated lysine residues of a transcription factor known to regulate innate T cell development, leading to its ubiquitination and degradation by the proteasome. Overall we have demonstrated that an HMTase can act in a chromatin-independent manner to fine tune trancription factor levels via methylation-dependent ubiquitination that ultimately controls innate T cell development and thus preserves immune homeostasis.