The induction of immune tolerance to dietary antigens and commensal microbiota relies on peripherally induced RORγt+ regulatory T cells (pTregs). While specialized RORγt+ antigen-presenting cells (APCs) have been implicated in this process, the developmental origin and specification of tolerogenic APCs that drive pTreg induction remain poorly defined. Here, we identify RORγt+ dendritic cells (DCs) as a distinct lymphoid-derived lineage whose development is essential for intestinal immune homeostasis. Using lineage tracing, single-cell transcriptomics, and in vitro and in vivo differentiation assays, we delineate a developmental trajectory originating from bone marrow resident Rorc(t)+ progenitors. These include a RORγt+ innate lymphoid progenitor (RILP), which generates both type 3 innate lymphoid cells (ILC3s) and RORγt+ DCs, and a pre-RORγt+ DC precursor committed exclusively to the RORγt+ DC lineage. Differentiation assays demonstrate that RORγt+ DCs arise predominantly from IL-7R+ lymphoid progenitors, which efficiently generate this lineage in culture and upon adoptive transfer, whereas myeloid progenitors show minimal potential. These findings establish RORγt+ DCs within the lymphoid branch of hematopoiesis. We further show that RORγt+ DC development is controlled by a defined transcriptional and epigenetic program. A cis-regulatory enhancer located +7kb downstream of the Rorc locus is required for the generation of both RILPs and pre-RORγt+ DCs, while its accessibility is regulated by the repressors REV-ERBα and REV-ERBβ. Downstream, the transcription factors PRDM16 and PU.1 enforce lineage commitment and enable progression into mature RORγt+ DC subsets. Disruption of this developmental program selectively abrogates RORγt+ DC differentiation, resulting in reduced pTreg induction and skewing toward T helper 2 responses. In contrast, selective loss of ILC3s does not recapitulate these defects, identifying RORγt+ DCs as the critical tolerogenic APC lineage. Together, these findings define an enhancer-driven developmental pathway linking lymphoid lineage specification to immune tolerance, positioning RORγt+ DCs as specialized regulators of intestinal homeostasis.