Pancreatic ductal adenocarcinoma (PDA) is a lethal and highly metastatic malignancy with limited response to surgery, chemotherapy, or immunotherapy. T cells function in an antigen-specific manner and are critical for tumor immune surveillance and clearance, making them frequent immunotherapy targets. Here, I investigate T cell responses in three different PDA murine models, reflecting the heterogeneity in human PDA. First, I mapped the differentiation trajectory of tumor-specific CD8 T cells in secondary lymphoid organs and tumor in response to anti-PDL1 and anti-CD40 immunotherapy. As this combination therapy failed to elicit durable responses in PDA clinical trials and only cures 50% of mice bearing neoantigen positive tumors I sought to identify T cell subsets mediating the immunotherapy induced antitumor response and pinpoint avenues for therapeutic improvement. For the first time in PDA, I identified a precursor stem-like subset of tumor-specific CD8 T cells which expanded with immunotherapy in response to tumor antigen and CD4 T cell help. I found IL-15 complex addition to anti-PDL1 + anti-CD40 cured 100% of mice in the neoantigen positive highly immunogenic model and elicited objective responses in the neoantigen low poorly immunogenic model. In both tumor models, treatmentwith triple therapy promoted a T-bet driven effector program while reducing Tox driven exhaustion across all CD8 T cell subsets. I next investigated a cancer cell intrinsic defect in MHC class I antigen presentation, which rendered cancer cells unrecognizable by CD8 T cells. I identified both CD8 T cells and CD4 helper T cells as defenders against cancer metastasis, while regulatory T cells suppress anti-tumor T cells and enable metastasis. CD4 T helper cell expansion and differentiation towards a Cxcr6+ effector program after regulatory T cell depletion or anti-CD40 agonist treatment abrogated metastasis and improved mouse survival. MHC class I expression rehabilitation synergized with CD4 T helper T cell engagement to cure 40% of mice and establish tissue resident memory CD4 and CD8 T cells. Thus, across immunogenically diverse PDA murine models I define critical pathways to enhance antitumor T cell function and identify phenotypic markers to delineate intratumoral T cell differentiation from tumor establishment to clearance.