Apoptosis and programmed necrosis (necroptosis) are cell death pathways with common signaling molecules, including Receptor-interacting protein kinase (RIP) 1, RIP3, and Caspase-8, which are critical for death receptor-induced apoptosis as well as necroptosis. Necroptosis is crucial during development and in response to viral infections. Here, we found a decreased frequency of iNKT cells in RIP3-/- Casp8-/- double-deficient (DKO) and RIP1-/- RIP3-/- Casp8-/- triple-deficient (TKO) mice in spleen as compared to RIP3-deficient or wild type mice. Thymic iNKT cell development was normal in RIP3-deficient and TKO mice when compared to wild type mice and so was iNKT cell activation as measured by CD69 and T-bet expression. However, we found a reduced proportion of NKT2 cells in the thymus of both RIP3-deficient and TKO mice as compared to wild type controls. In peripheral organs, TKO mice had a significant decrease in the proportion of iNKT cells, and remaining iNKT cells expressed lower levels of CD69 and T-bet, as compared to wild type or RIP3-deficient mice. Splenic neutrophils from TKO mice expressed significantly lower levels of CD1d, as compared to RIP3-/-, DKO, or wild type mice, indicating that RIP1 is required to equip neutrophils for cognate engagement of iNKT cells. In summary, our data suggests that apoptosis is required to maintain thymic iNKT subsets as well as peripheral iNKT cell homeostasis and activation. Additionally, RIP1 is specifically required for neutrophil CD1d expression, thereby enabling interaction with iNKT cells.