Social anxiety disorder (SAD) is caused by stressful social encounters. The Social Fear conditioning (SFC) paradigm is able to effectively simulate the symptoms of social phobia, such as a severe fear and avoidance of social situations. The extinction phase of the SFC paradigm mimics exposure therapy for SAD and facilitates the learning of the disassociation between the trauma and the social context. The lateral septum (LS), known to be involved in socio-emotional regulation, abundantly expresses corticotropin-releasing factor receptors (CRFR1/CRFR2) and several lines of evidence implicate the CRF system in regulating anxiety, and social behavior. RNAscope analysis of the LS showed highest concentration of CRFR1 and CRFR2 expressing cells in the medial part of the LS. Following up on these data, we pharmacologically manipulated both LS-CRFR2 neurons by infusing either a CRFR2 agonist (Urocortin 3), antagonist (Astressin-2B), or CRFR1 agonist (CRH) before extinction to determine the effect of LS-CRFR1/2 signaling on social fear extinction and circulating corticosterone levels. We demonstrated that activation of LS-CRFR2 neurons facilitates the extinction of social fear and elevates the circulating corticosterone levels, but activation of LS-CRFR1 signaling neurons impairs social fear extinction. Our results indicate that the CRFR1/2 signaling within the LS may have two pathways that are engaged in a synchronized and opposing manner in the stress-induced regulation of social fear extinction and HPA axis response.