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 (<italic>TCR</italic>) and immunoglobulin (<italic>Ig</italic>) genes. Although <italic>Rag1</italic> and <italic>Rag2</italic> expression is largely restricted to adaptive lymphoid lineage cells, it remains unclear how <italic>Rag</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 (<italic>R-TEn</italic>) and the two B cell–specific elements, <italic>R1B</italic> and <italic>R2B</italic>. By generating mice lacking either <italic>R-TEn</italic> or <italic>R1B</italic> and <italic>R2B</italic>, we demonstrate that these distinct sets of regulatory elements drive the expression of <italic>Rag</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 <italic>R-TEn</italic>, we demonstrate that recruitment of E2A to this site is essential for orchestrating changes in chromatin conformation that drive expression of <italic>Rag</italic> genes in T cells. By mapping cis-regulatory elements and generating multiple mouse strains lacking distinct enhancer elements, we demonstrate expression of <italic>Rag</italic> genes in developing T and B cells to be driven by distinct sets of E2A-dependent cis-regulatory modules.