<jats:p>Cell type–specific gene expression is driven by the interplay between lineage-specific transcription factors and cis-regulatory elements to which they bind. Adaptive immunity relies on RAG-mediated assembly of T cell receptor (<jats:italic>TCR</jats:italic>) and immunoglobulin (<jats:italic>Ig</jats:italic>) genes. Although <jats:italic>Rag1</jats:italic> and <jats:italic>Rag2</jats:italic> expression is largely restricted to adaptive lymphoid lineage cells, it remains unclear how <jats:italic>Rag</jats:italic> gene expression is regulated in a cell lineage–specific manner. Here, we identified three distinct cis-regulatory elements, a T cell lineage–specific enhancer (<jats:italic>R-TEn</jats:italic>) and the two B cell–specific elements, <jats:italic>R1B</jats:italic> and <jats:italic>R2B</jats:italic>. By generating mice lacking either <jats:italic>R-TEn</jats:italic> or <jats:italic>R1B</jats:italic> and <jats:italic>R2B</jats:italic>, we demonstrate that these distinct sets of regulatory elements drive the expression of <jats:italic>Rag</jats:italic> genes in developing T and B cells. What these elements have in common is their ability to bind the transcription factor E2A. By generating a mouse strain that carries a mutation within the E2A binding site of <jats:italic>R-TEn</jats:italic>, we demonstrate that recruitment of E2A to this site is essential for orchestrating changes in chromatin conformation that drive expression of <jats:italic>Rag</jats:italic> genes in T cells. By mapping cis-regulatory elements and generating multiple mouse strains lacking distinct enhancer elements, we demonstrate expression of <jats:italic>Rag</jats:italic> genes in developing T and B cells to be driven by distinct sets of E2A-dependent cis-regulatory modules.</jats:p>