Steady state IL-4 production by a unique subset of iNKT cells (NKT2) in the thymus conditions CD8⁺ T cells to become “memory like”. However, the signals that cause NKT2 cells to constitutively produce IL-4 and what additional influence this has in the thymus are poorly defined. Using histocytometry, IL-4 producing NKT2 cells were localized to the thymic medulla, and depletion of medullary thymic epithelial cells (mTEC) using Aire-DTR mice resulted in a dramatic loss of IL-4 production. NKT2 cells express and require IL-17RB, the receptor for IL-25. Thus we examined mTEC using IL-25 reporter “FLARE” mice, and observed a distinct sub-population of chemosensory “tuft-like” cells that constitutively express IL-25 in the medulla.  Using pouf3^-/- and DLCK^CreRosaDTA mice, we showed these cells are required for IL-4 production in NKT2 cells. We also show here that NKT2 cells require TCR stimulation for continuous IL-4 production, as NKT2 cells lost Nur77^GFP and IL-4 production when intra-thymically transferred to CD1d deficient hosts. However, in bone marrow chimeric hosts, only hematopoietic, not stromal APC, provided such stimulation. These data suggest that NKT2 cells require factors from multiple APC in the thymic medulla for IL-4 production. In addition to conditioning CD8⁺ T cells, we show that NKT-derived IL-4 influences class switching in thymic B cells, medullary organization, and the composition of thymic macrophages. The challenge going forward is to understand what type of ligands NKT2 respond to and why this response dramatically shapes lymphocyte development.