Dendritic cells (DCs) are key antigen-presenting cells comprising of functionally and phenotypically distinct subsets. DCs are rare in tumors where their heterogeneity remains unclear. To overcome the limitations of surface marker-based analyses, we utilized genetically engineered DC-reporter mice (Zbtb46GFP/+) to isolate tissue and tumor DCs and performed single-cell RNA sequencing (scRNA-seq). Through the scRNA-seq approach, the major ontogenic DC subsets (cDC1 and CD11b+ DC2) were identified along with two activated DC states. One activated state displayed a hallmark DC migratory program (migratory DC or mDC) and showed superior T cell stimulatory properties. Notably, tumors, but not steady-state tissue, also harbored a distinct state of activated DCs that lacked a migratory program, instead displaying signature of clear interferon exposure (interferon-DC or IFN-DC). IFN-DCs supported T cell proliferation and expressed T cell-recruiting chemokines. Using a combination of genetic, pharmacologic, and computational approaches, we further showed that type I and II interferons can activate DC2s into IFN-DCs in the tumor. Furthermore, analysis of DCs from an aggregated human mononuclear phagocyte scRNA-seq dataset revealed a similar split in migratory or IFN response modules among human tumor DCs. A classic dogma in the field is that DCs migrate to draining lymph nodes upon activation, however our data suggests chronic tumor inflammation with IFN signaling can also induce activated DCs that are not primed to migrate. Taken together, our findings illuminate DC heterogeneity in tumors and suggest different scenarios of DC activation, including a spatiotemporal ‘division of labor’ among activated DCs, whereby mDCs migrate to and drive T cell priming in draining lymph nodes while IFN-DCs help recruit and support activated T cells within the tumor microenvironment. This opens new avenue of research into functional specialization of DCs and can support efforts on targeting different DC subsets and states for DC-based immunotherapy.