Human iNKT cells can be broadly divided on the basis of CD4 expression, with CD4-negative iNKT cells displaying a TH1/cytolytic profile, while the CD4+ subset appears appears more polyfunctional and has both regulatory and immunostimulatory characteristics. It was therefore not surprising that the CD4-negative iNKT cells successfully limited the growth of human lymphoblastoid spheroids in vitro, whereas CD4+ iNKT cells showed little or no direct anti-tumor activity. However, we were surprised to find that the anti-tumor effects of the two subsets were completely reversed when we tested them as adoptive immunotherapies in vivo using a xenograft model of human B cell lymphoma. CD4-negative iNKT cells had no discernable impact, whereas CD4+ iNKT cells produced a rapid reduction in tumor mass that appeared to be due to adjuvancy effects on conventional T cells. Investigation of CD4+ iNKT cell adjuvancy revealed that they form stably adhered bi-cellular complexes with monocyte-derived DCs that migrate together as pairs and show extended DC calcium signaling. The iNKT-DC complexes showed upregulated expression of multiple key co-stimulatory molecules and were efficient activators of CD8+ T cells. Moreover, administering iNKT-DC complexes as a cellular immunotherapy was highly effective at late stages of tumor progression that were refractory to immune checkpoint blockade immunotherapy, suggesting that the consortium of activating signals provided by iNKT-DC complexes rejuvenates exhausted anti-tumor immunity. Together these results highlight the immunotherapeutic potential of iNKT-mediated adjuvancy for treating human cancer.