Although monocyte-derived dendritic cells (DCs) have been extensively trialled as tumour “vaccines” with limited success, recent evidence indicates that type 1 conventional DCs (cDC1s) are most effective at promoting anti-tumour immunity. Intrinsic dysfunction or deficiency of cDC1s impairs the immune system’s ability to control or reject transplanted tumours. Tumour cells can evade recognition by cDC1s through downregulation of tumour-specific antigens or by expressing heterogeneous antigens across different tumour cells. To enhance cDC1 recognition of low-abundance tumour-specific antigens and uptake of heterogeneous tumour-associated antigens, we engineered a chimeric antigen receptor (CAR) targeting HER2, incorporating the TIR domain of TLR4, and transduced it into cDC1s. The functional domain structure of the CAR remained intact after recombination. Introducing the CAR into cDC1s significantly increased their affinity for tumour-specific antigens and enhanced their phagocytic capacity for apoptotic bodies derived from tumour cells. The cross-presentation of antigens was improved upon stimulation of CAR-cDC1s with apoptotic tumour cells. Importantly, the CAR, which targets a known tumour-associated antigen, enabled cDC1s to capture and present novel tumour-specific antigens, thereby priming T cells. Transduction with the TIR-CAR resulted in the upregulation of co-stimulatory molecules and the secretion of pro-inflammatory cytokines, thereby promoting robust T cell responses. Furthermore, we developed a protocol for the efficient generation of human CAR-cDC1s without compromising their viability. We observed that these CAR-cDC1s demonstrated tumour-associated antigen recognition and antigen-dependent activation of cDC1s. Here, we propose a potentially first-in-class cell therapy platform to meet the urgent clinical need for treating cancer patients who are unresponsive to current therapies, especially those with intractable solid cancers.