CD1d-restricted invariant (i)NKT cells participate in cancer immune surveillance but their site and mechanisms of action are incompletely understood. We investigated the oncogene induced mouse prostate cancer (PC) model TRAMP, in which the absence iNKT cell resulted in more aggressive tumors and decreased survival. iNKT cells actively remodelled the TRAMP tumor microenvironment (TME). iNKT cell deficiency subverted the tumor microenvironment, promoting pro-angiogenic and immunosuppressive programs in infiltrating CD45⁺ cells, and resulted in a significant expansion of pro-angiogenic tumor associated macrophages (TEMs), and reduction of the pro-inflammatory ones. Reduced iNKT cells, and increased TEM and pro-angiogenic signatures, characterized also aggressive human PCs. iNKT cells localized in the tumor stroma in direct contact with macrophages and their transfer in tumor-bearing mice restricted TEMs, restored the tumor associated macrophage (TAM) balance, and delayed tumor progression. TAM modulation by iNKT cells required the combinatorial engagement of CD1d, CD40 and Fas, which promoted selective killing of the pro-angiogenic population and survival of the pro-inflammatory one. These results suggested that iNKT cells may be utilized as a cellular platform to therapeutically reprogram the TME and enforce tumor-opposing functions, which is critical for the successful outcome of the current immunotherapy approaches. To this aim, we sought to engineering iNKT cells with TCRs specific for MHC-restricted peptides derived from tumor-associate antigens (TAAs), in order to achieve dual targeting of TEMs and cancer cells with a single immune effector upon adoptive immunotherapy. We could transduce mouse iNKT cells in vitro with exogenous TCRs specific for epitopes derived from gp100, Ova or SV40LT tumor antigens which are variably co-expressed with the endogenous invariant TCR. Engineered iNKT cells are dual functional and specifically recognize CD1- and MHC-restricted ligands in vitro. Their therapeutic activity is currently being investigated in vivo against different types of transplantable mouse tumors expressing the cognate antigens.