iNKT cells are implicated in the control of different tumors through direct and indirect mechanisms. We previously showed that lack of iNKT cells from transgenic adenocarcinoma of the mouse prostate (TRAMP-Jα18^-/-, TRAMP-CD1d^-/-) results in more precocious and aggressive prostate cancers (PC), leading to reduced survival compared to iNKT-cell sufficient TRAMP animals. Here, we investigated the mechanisms underpinning the iNKT cell control of mouse PC progression in two models: 1. TRAMP mice; 2. sc tumors induced by the injection of the TRAMP-C1 prostate cancer cell line, which also grow faster in mice lacking iNKT cells. In both tumor types, we find a significant increase of angiogenesis and pro-angiogenic Tie-expressing tumor infiltrating macrophages (TEMs, M2-like), and decrease of pro-inflammatory CD11c⁺ tumor associated macrophages (CD11c⁺TAMs, M1-like), in iNKT cell-deficient hosts compared with WT mice. iNKT cell transfer into iNKT cell-deficient tumor bearing mice decreases TEMs, reverts the balance towards CD11c⁺-TAMs and delays tumor progression. Tumors contain spontaneously infiltrating iNKT cells, while the transferred iNKT cells are retrieved in the tumor beds of iNKT cell-deficient mice, supporting a local action. Modulation of TAMs in vivo critically depends on CD1d cognate recognition and on iNKT cell expression of CD40L and FASL, but not of IFN. Upon co-cultures in vitro with BM-derived macrophages, iNKT cells sustain M1 macrophage survival via the CD40L-CD40 pathway; selectively kill M2 cells via the FasL-Fas engagement; polarize M0 into M1 macrophages. Collectively, these results highlight a new mechanism whereby iNKT cells restrain initial PC progression and angiogenesis via non-redundant mechanisms that differentially modulate TAM subsets, resulting in the generation of a pro-inflammatory/tumor-contrasting microenvironment.