Effective induction of anti-tumor immunity requires dendritic cells (DCs) to internalize, process and present tumor antigens to T cells. However, the hostile tumor microenvironment (TME) impedes this process by suppressing DC maturation and antigen presentation through several mechanisms. Adoptive transfer of DCs matured and pulsed with lysed cancer cells or defined antigens ex vivo may help to circumvent the suppressive TME. While this method, often called "DC vaccine", has been tested in numerous clinical trials, it has often failed to yield frequent and durable clinical responses. Using DC maturation cocktails prior to injection shortens the life span of adoptively transferred DCs, which limits their ability to present antigens to tumor-reactive T cells. Moreover, cancer cells exhibit altered proteasome functions that cleave antigens differently from activated DCs. Therefore, DCs pulsed with tumor lysates/antigens may load their MHCI molecules with antigen epitopes that differ from those of the cancer cells, leading to inefficient T cell priming. Additionally, this method requires tumor biopsies to be obtained, which may not be feasible for certain tumors and metastatic lesions. To overcome the limitations of traditional DC vaccines, we devised a new DC-based immunotherapy strategy that allows adoptively transferred DCs to bind to tumor-derived extracellular vesicles (EVs) and acquire tumor-derived peptide-MHCI complexes present on the tumor EVs. This would obviate the need to obtain tumor biopsies and enables T cell presentation of tumor antigen epitopes found on tumor cells. To accomplish this, we designed an inducible EV internalizing receptor (iEVIR) which enables DCs to bind to a certain surface tumor antigen, such as HER2 or GD2. To circumvent the need to mature DCs prior to injection, the iEVIR was designed to promote DC activation upon binding to cancer cells or tumor-derived EVs, synchronizing antigen uptake with DC activation. Our in vitro assays show that the expression of iEVIR in DCs enhances tumor-derived EV uptake concurrently with enhancement of DC activation. Furthermore, we demonstrate that iEVIR-expressing DCs cross-dress peptide-MHCI complexes from tumor-derived EVs and robustly enhance antigen-specific T cell proliferation and activation in vitro. We also show that injection of iEVIR-expressing DCs delays tumor growth in mice bearing B16F10 melanomas, extending their survival. We further demonstrate that an improved version of the iEVIR, made resistant to ubiquitination and degradation, called UB null iEVIR, improves DC cross-dressing with tumor antigens in vitro. In tumors, adoptively transferred DCs expressing the UB null iEVIR increase the abundance of tumor-reactive CD8 T cells. Finally, we designed an inducible promoter that is activated specifically upon engagement of and signaling from the iEVIR. This system, named "Super iEVIR", enables DCs to express a molecule of interest "on demand", that is only upon contact with cancer cells or tumor-derived EVs.