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APCs are essential for the orchestration of antitumor T cell responses. Batf3-lineage CD8α+ and CD103+ dendritic cells (DCs), in particular, required spontaneous initiation CD8+ priming against solid tumors. In contrast, little is known about that regulate responses hematological malignancies. Using an unbiased approach, we aimed to characterize responsible regulating a syngeneic murine leukemia model. We show with single-cell resolution DCs alone acquire cross-present Ags vivo, culminating induction leukemia-specific tolerance. Furthermore, demonstrate mere acquisition cargo associated unique transcriptional program may be important tolerogenic DC functions mice leukemia. Finally, systemic activation TLR3 agonist completely prevents their ability generate tolerance resulting instead potent antileukemia immunity prolonged survival leukemia-bearing mice. Together, our data reveal imprint disparate fates hosts tumors versus