Successful immune checkpoint blockade (ICB) response depends on the generation and persistence of progenitor-exhausted T cells (Tpex), which are TCF-1+ stem-like CD8 T cells that self-renew and give rise to more differentiated effector progeny that eventually eradicate tumor cells. Emerging evidence suggests that conventional type 1 dendritic cells (cDC1) are crucial for priming and sustaining these Tpex populations, and reduced cDC1 abundance or function may limit ICB efficacy. By integrating single-cell RNA sequencing datasets of tumor-infiltrating lymphocytes in human head and neck squamous cell carcinoma (HNSCC), we discovered that cDC1s uniquely express the chemokine receptor XCR1, whose cognate ligands (XCL1 and XCL2) are mainly produced by natural killer (NK) cells and certain CD8 T cell subsets. To harness this chemokine signaling axis, we engineered ssXCL1, a hyperactive form of XCL1 that has an agonist activity ~100-fold greater than wild-type XCL1. Local delivery of ssXCL1 to the tumor increases intratumoral cDC1 and CD8 T cell numbers and diminishes T cell exhaustion. ssXCL1 treatment was ineffective in XCR1-/- mice, confirming on-target specificity through XCR1 signaling. When combined with systemic anti-PD-1 therapy, ssXCL1 significantly increased the treatment response rate from 20% to 60%. Spatial analysis of human HNSCC tissues revealed critical cDC1-CD8 T cell niches where XCL1-expressing CD8 T cells express Tpex signature. Our findings provide encouraging evidence that ssXCL1’s action critically depends on XCR1 signaling and that the chemokine-driven cDC1 recruitment to the tumor lesions is sufficient to reactivate the cancer-lymphatic immune cycle. Furthermore, these studies raise the possibility of harnessing the cancer immune chemokine network as a compelling strategy to enhance current ICB immunotherapies and establish complete, long-term antitumor immunity.