ADAR1 is a crucial innate sensor that discriminates between self and non-self by binding and editing dsRNA species. Previous work has established that loss of tumoral ADAR1 results in extensive remodeling of the immune compartment in the tumor microenvironment. However, the effects of tumor-intrinsic dsRNA sensing on antigen-specific T cell immunity remain to be elucidated. Using murine melanoma models, we found increased infiltration of antigen-specific CD8+ T cells that are required for tumor regression and survival observed following loss of tumoral ADAR1. In addition, we found an increased infiltration of both DC1s and DC2s in Adar1-null tumors compared to control on day 14. Further characterization of Adar1-null intratumoral cDCs revealed high expression of co-stimulatory molecules, CD80 and CD86, maturation marker CCR7, and phagocytic receptor AXL compared to control cDCs, consistent with what we observed in in vitro co-culture assays using bone marrow-derived DC1s and DC2s (BMDCs). When in co-culture with Adar1-null tumor cells, we found that b2m-deficient BMDCs MHCI-dress in a type I interferon-dependent manner, accordant with single cell RNA sequencing data showing ISG DCs in Adar1-null B16 tumors, but not in control tumors. While BMDCs cultured with Adar1-null tumor cells induced naïve OTI T cell proliferation significantly more than BMDCs cultured with control B16 tumor cells, we were surprised to find that depletion of cDCs had no significant effect on tumor growth and survival of Adar1-null tumor-bearing mice, suggesting other cell types may be priming naïve OTI T cells in vivo. Interestingly, in vitro co-culture experiments show Adar1-null tumors can directly prime naïve OTI T cells. Ongoing ex vivo co-culture assays aim at identifying the cell type responsible for priming naïve T cells in the absence of DCs and downstream consequences on T cell phenotype. Our work demonstrates loss of ADAR1 in tumors induces non-canonical antigen-specific T cell activation.