Differentiation of proinflammatory CD4 conventional T?cells (T) is critical for productive antitumor responses yet their elicitation remains poorly understood. We comprehensively characterized myeloid cells in tumor draining lymph nodes (tdLN) of mice and identified two subsets of conventional type-2 dendritic cells (cDC2) that traffic from tumor to tdLN and present tumor-derived antigens to CD4 T， but then fail to support antitumor CD4 T differentiation. Regulatory T?cell (T) depletion enhanced their capacity to elicit strong CD4 T responses and ensuing antitumor protection. Analogous cDC2 populations were identified in patients， and as in mice， their abundance relative to T predicts protective ICOS PD-1 CD4 T phenotypes and survival. Further， in melanoma patients with low?T abundance， intratumoral cDC2 density alone?correlates with abundant CD4 T and with responsiveness to anti-PD-1 therapy. Together， this highlights a pathway that restrains cDC2 and whose reversal enhances CD4 T abundance and controls tumor growth.