Immunotherapies have shown significant benefits in clinical settings, offering hope to cancer patients. Therapeutic cancer vaccines aim to induce tumor regression, eradicate minimal residual disease, establish lasting anti-tumor memory, and avoid non-specific or adverse reactions. However, challenges remain, such as low immune responses and immune evasion mechanisms employed by cancer cells, like downregulated MHC expression. These inadequate immune responses can contribute to immunoediting, leading to the selection of resistant cancer cell clones. Therefore, enhancing the immune response is a primary focus. Herein, we developed a nanoshell vaccine combining PLGA hollow nanoparticles and an adaptor-peptide design to bypass intracellular processing and induce robust T cell responses. Compared to other vaccines for HPV+ tumors and prostate cancer, the nanovaccine induces a more robust and durable antigen-specific CD8+ T cell response, resulting in superior tumor clearance. Furthermore, the nanovaccine effectively counters tumor MHC downregulation-mediated tumor immune evasion. The high levels of antigen-specific CD8+ T cells can reverse MHC downregulation in neighboring tumor cells by secreting IFNγ, converting the tumor microenvironment into an immunogenic state, and eliminating resistant tumor clones. With its excellent biosafety profile and superior ability to induce potent CD8+ T cell responses, the nanovaccine offers a versatile platform for therapeutic cancer vaccines.