During immune responses, naive CD4+ T lymphocytes differentiate into functionally distinct stable T helper (Th) cell subsets under the control of lineage-specifying genes. The stability of Th cell differentiation is critical to their functions both in protective immune responses and inflammatory diseases. Here, we explored the role of the Suv39h1-H3K9me3-HP1a epigenetic pathway of gene silencing in the control of Th2 lineage stability. In Th2 cells deficient for Suv39h1, the ratio between the trimethylation and acetylation of H3K9 is impaired, and the binding of HP1a at silenced promoters of Th1 genes is reduced. Despite displaying normal differentiation, both Suv39h1- and HP1a-deficient Th2 cells expressed Th1 genes upon re-culture in Th1 conditions. In a murine model of Th2-driven allergic asthma, the loss of Suv39h1 resulted in skewing towards a Th1 response in vivo and decreased lung pathology. We propose that the Suv39h1-HP1a pathway participates in maintaining a silent state of the Th1 loci to ensure Th2 lineage stability.