Adoptive cell transfer (ACT) therapy using patient-derived T cells genetically engineered to express a chimeric antigen receptor (CAR) is highly effective in B cell malignancies and is now FDA-approved. However, tumour heterogeneity remains a major challenge in treating solid tumours due to the relapse of tumours negative for CAR-targeted antigen. Previously we demonstrated that CAR T cells engineered to secrete (DC) growth factor Fms-like tyrosine kinase 3 ligand (Flt3L) promote host anti-tumour immunity to effectively eradicate heterogenous tumours by expanding intratumoural conventional type 1 dendritic cells (cDC1) (Lai et al. 2020 Nat Immunol). cDC1 is well-reported to be a critical mediator in activation of anti-tumour cytotoxic responses. A key aspect of this study was that despite the increased population of intratumoral cDC1s, cDC1s required a second activatory stimulus to elicit anti-tumour immunity. Here, we explored the possibility of leveraging the CD40 axis to promote cDC1 function and synergise with Flt3L-secreting ACT therapy. Engagement of upregulated CD40 on antigen-experienced DC with its ligand CD40L, which is traditionally expressed on activated T cells, induces DC activation. The effect of activation was observed via the upregulation of co-stimulatory molecules, CD80 and CD86, indicating DC maturation and expansion of tumour-antigen specific T cells upon anti-CD40 activation of Flt3L-expanded cDC1 in vivo. To incorporate the CD40 axis activation in adoptive cell therapy, successful engineering of CAR T cells was conducted using a novel construct to induce high CD40L expression constitutively. Improved DC maturation was observed upon CD40 engagement following adoptive transfer of CD40L-expressing T cells, correlated with improved therapeutic efficacy. Based on our results of the synergistic effect between Flt3L and CD40L on cDC1, we are poised to further incorporate this with Flt3L-secreting CAR T cell to achieve cDC1 expansion and activation upon ACT. Our study has demonstrated an enhanced efficacy of CAR T cell treatment in solid cancers by harnessing the endogenous immune responses against tumours.