Dendritic cells (DCs) are key regulators of responsiveness to immunotherapies and protective immune responses to cancer. We, and others, have shown that type 1 conventional dendritic cells (cDC1s) promote protective immune responses to cancer and are key regulators of patient responses to anti-PD-1 immune checkpoint blockade immunotherapy. cDC1 abundance in the tumor is controlled by the cytokine Fms-related tyrosine kinase 3 ligand (FLT3LG in humans/Flt3L in mice) which is produced by innate lymphocytes called natural killer (NK) cells. In this study, we show that NK cell production of Flt3l in the tumor is regulated by activation and that activation by IL-2 and IL-15 uniquely induced Flt3L expression in NK cells. In melanoma, IL-2 signaling in NK cells led to increased Flt3L production, which boosted cDC1 abundance in the tumor and improved anti–PD-1 immunotherapy response. Furthermore, NK cell subsets differentially regulated Flt3l in the tumor, with CD11b⁻CD27⁺ NK cells in mouse tumors enriched for IL-2 family signaling and up-regulating Flt3l upon activation. Consistently, human CD56^brightCD16⁻ NK cells more strongly correlated with cDC1 and FLT3LG expression than other NK cell subsets across multiple human melanoma datasets and cancer indications. Furthermore, cDCs appear to be the dominant cell type producing IL-15 in the tumor, suggesting a feed forward mechanism where cDC1s generate IL-15 to induce FLT3LG production, thereby increasing their survival and boosting protective anti-tumor immune responses. This mechanistic study of the regulation of the NK cell - cDC1 innate immune axis provides insights and strategies for the development of more effective cancer immunotherapies that target the abundance of protective cDC1s in the tumor.