CD8⁺ T cells are a critical component of the cellular response to intracellular pathogens such as viruses. The differentiation of naïve CD8⁺ T cells into effector cells after activation is accompanied by large scale changes to the epigenetic and chromatin landscape, ultimately resulting in transcriptional, phenotypic and functional differences. SATB1 is a master regulator of chromatin structure and a key for directing T cell lineage-specific transcriptional programs during immature T cell development. To examine whether SATB1 plays a role in mature CD8⁺ T cell specification and optimal virus-specific responses, we first demonstrated that SATB1 is highly expressed in both mouse and human, naïve CD8⁺ T cells, and is down-regulated upon effector T cell differentiation. SATB1 imposter mice (SATB1^imp/imp) exhibit a point mutation in the SATB1 chromatin binding domain that results in less efficient SATB1 targeting to the genome. While SATB1^imp/imp CD8⁺ T cells exhibited similar cellular proliferation and granzyme expression to wildtype (WT) CD8⁺ T cells after in vitro activation, CD44 upregulation and CD62L downregulation was altered. Strikingly, primary respiratory infection with influenza A virus (IAV) of SATB1^imp/imp mice showed fewer IAV-specific CD8⁺ effector T cells in the lung compared to WT mice. RNA sequencing analysis demonstrated that SATB1^imp/imp naïve CD8⁺ T cells exhibited increased levels of γδ TCR transcripts, that were over-represented in the responding IAV-specific CD8⁺ T cells. In contrast, WT IAV-specific CD8⁺ T cells exhibited conventional αβ TCR repertoires. Moreover, naïve SATB1^imp/imp CD8⁺ T cells exhibited higher mRNA levels of genes encoding immune inhibitory receptors such as Pdcd1, Ctla4 and Lag3. Given the role of these molecules in limiting T cell function, it is tempting to speculate that the higher transcript levels impose limits on in vivo IAV-specific primary T cell expansion and/or recruitment at the site of IAV infection.