Lesion and inactivation studies indicate that the central amygdala (CeA) participates in the expression of cued and contextual fear, whereas the bed nucleus of the stria terminalis (BNST) is only involved in the latter. The basis for this functional dissociation is unclear because CeA and BNST form similar connections with the amygdala and brainstem fear effectors. To address this question, we recorded neurons in the anterolateral (AL) and anteromedial (AM) regions of BNST in rats subjected to auditory fear conditioning. During habituation, few neurons were responsive to the conditioned stimulus (CS). After fear conditioning, 20% of BNST-AL neurons developed inhibitory responses to the CS. In BNST-AM, 26% of neurons developed positive CS responses. The behavior of BNST-AM and -AL neurons during contextual fear paralleled their CS responsiveness: More BNST-AM neurons fired at higher rates during contextual freezing than movement, whereas the opposite was seen in BNST-AL cells. These findings point to regional differences in the activity of BNST-AL and -AM in relation to learned fear, raising the possibility that they exert opposite influences on fear output networks. However, given the similar behavior of BNST-AM and -AL neurons in relation to cued and contextual fear, it remains unclear why lesion and inactivation of BNST differentially affect these two types of fear. Either neurons in a different BNST sector, not explored here, show a different activity profile in relation to the two forms of fear or inactivation/lesion studies inadvertently affected a structure adjacent to BNST, which is involved in contextual fear.