Abstract RORγt is the transcription factor responsible for the development and function of T helper 17 (Th17), γδT17, and innate lymphoid cells (ILC3s), which are key drivers of both immunity in tissues proximal to barrier surfaces and of autoimmune pathogenesis. An understanding of how regulation of the RORγt locus contributes to the programming of these separate lineages is crucial to dissecting the confounding ability of RORγt to drive such divergent responses. Examination of mice deficient in individual transcription factors that we found to constitute a key regulatory module driving Th17 cell development revealed divergent control of RORγt in innate and adaptive immune cells. This evidence suggests that distinct genomic cis-acting regulatory elements drive RORγt expression in a context dependent manner. Indeed, we found that cell-specific combinatorial usage of enhancers regulates the development and function of RORγt+ lineages in-vivo. Specifically, Th17 and ILC3 have largely unique enhancer usage while innate-like gdT17 cells share both innate and adaptive elements. We show that in vivo deletion of individual enhancer elements can modulate RORγt expression in a cell-type specific manner, the tuning of which affects cell frequency and function. Our findings provide new opportunities to study the contributions of individual RORγt+ lineages to immunity and inflammation. Moreover, these enhancers, which are highly conserved in humans, can be used to locate novel polymorphisms involved in the stratification of RORγt-dependent disease.