Invariant natural killer T (iNKT) cells are a subset of innate-like T lymphocytes with a limited TCR repertoire that recognize glycolipid antigen presented on the MHC-I-like molecule CD1d. iNKT cells produce a broad range of cytokines upon activation and play an essential role in directing the cytokine response. In addition to guiding the immune response, iNKT cells can mount strong antitumor responses via interferon γ production, underscoring the importance of understanding how iNKT cells develop and mature into effector populations. Using a novel model for conditional deletion of transcription factor ETS1 in iNKT1 cells, I show that ETS1 regulates the adhesion gene program of iNKT1 cells, promoting a more epithelial transcriptome profile. This is achieved, in part, by suppressing expression of the transcription factor T-bet. T-bet promoted the expression of migration genes S1pr1 and S1pr5 and repressed classical iNKT liver retention mediated by LFA-1 and ICAM-1. In the thymus, ETS1 promoted optimal iNKT1 cell numbers. Conditional knockout of TGF-β signaling in iNKT1 cells suggests that expression of adhesion receptors CD49a and CD103 are important in thymic iNKT1 cell maturation. As a similar phenotype was observed in Ets1Δ/Δ thymic iNKT1 cells, ETS1 may regulate CD49a and CD103 expression by promoting optimal TGF-β signals. Together, I conclude that ETS1 has tissue-specific functions in iNKT1 cells; supporting proper maturation in the thymus and enforcing a more NKT-like adhesome expression profile to support classical retention in the liver.