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The therapeutic efficacy of whole tumor cell vaccines (TCV) is modest, which has delayed their translation into personalized immunotherapies in the clinic. Here, we developed an innovative and highly potent TCV platform based on photothermal nanoparticle-loaded tumor cell, which could be rationally applied to diverse tumor types to achieve on-demand boost of anti-tumor immune responses for effectively suppressing tumor growth. During the fabrication process, mild photothermal heating by near-infrared (NIR) laser irradiation induced the nanoparticle-bearing tumor cells to express heat shock proteins as endogenous adjuvants. After a single vaccination, non-invasive NIR laser irradiation further induced mild hyperthermia at vaccination site, which promoted the recruitment, activation, and presentation of dendritic cells. Notably, using a new indicator we termed fluctuation of tumor growth rate (FTGR), we rationally determined appropriate irradiation regimens (including optimized irradiation intervals and times). This innovative TCV platform enables on-demand NIR manipulation of immune responses, and we systematically demonstrated potent therapeutic efficacy against six murine models that mimicked a range of clinical requirements, notably including a sophisticated model based on humanized mice and patient-derived tumor xenografts.