Langerhans cells (LCs) are long-lived, self-renewing tissue-resident antigen-presenting cells that form dense networks in stratified epithelia and migrate to draining lymph nodes to maintain immune tolerance. LC development and maintenance of their immature-epithelial identity depend on TGF-β family signaling, yet the transcriptional mechanisms downstream of this pathway remain poorly understood. Here, we identify the basic helix-loop-helix transcription factor BHLHE40 (DEC1) as a positive regulator of epithelial LC differentiation. Transcriptomic profiling of an in vitro LC differentiation system from human hematopoietic progenitors revealed rapid induction of BHLHE40 downstream of TGF-β1–TGFBR1/ALK5 signaling in monocyte-committed precursors. Lentiviral perturbation demonstrated that BHLHE40 promotes LC differentiation, while its loss skews cells toward a monocyte fate. Mechanistically, BHLHE40 enhanced transcriptional programs linked to epithelial adaptation and immunoregulation, including upregulation of epithelial adhesion molecules and downregulation of monocyte signatures. In human skin, BHLHE40 is widely expressed in steady-state LCs but reduced in psoriatic monocyte-derived LCs, consistent with IL-4–mediated repression observed during monocyte derived DC differentiation. Supporting a conserved role in vivo, Bhlhe40-deficient mice exhibit disruption of the epidermal LC network and reduced LC accumulation in skin-draining lymph nodes. Together, these findings establish BHLHE40 as a conserved regulator connecting canonical TGF-β1 signaling to epithelial LC homeostasis.