Chronic epithelial injury triggers a TGFβ-mediated cellular transition from normal epithelium into a mesenchymal-like state that produces subepithelial fibrosis and airway remodeling. Here we examined how TGFβ induces the mesenchymal cell state, and determined its mechanism. We observe that TGFβ stimulation activates an inflammatory gene program controlled by the NFB/RelA signaling pathway. In the mesenchymal state, NFB-dependent immediate-early genes accumulate euchromatin marks and processive RNA polymerase. This program of immediate-early genes is activated by enhanced expression, nuclear translocation and activating phosphorylation of the NFB/RelA transcription factor on Ser 276, mediated by a paracrine signal. Phospho-Ser 276 RelA binds to the BRD4/CDK9 transcriptional elongation complex, activating the paused RNA Pol II by phosphorylation on Ser 2 in its carboxy terminal domain (CTD). RelA-initiated transcriptional elongation is required for expression of the core EMT transcriptional regulators SNAI1, TWIST1 and ZEB1 and mesenchymal genes. Finally, we observed that pharmacological inhibition of BRD4 can attenuate experimental lung fibrosis induced by repetitive TGFβ challenge in a mouse model. These data provide a detailed mechanism for how activated NFB and BRD4 control EMT initiation and transcriptional elongation in model airway epithelial cells in vitro and in a murine pulmonary fibrosis model in vivo. Our data validates BRD4 as an in vivo target for the treatment of pulmonary fibrosis associated with inflammation-coupled remodeling in chronic lung diseases.