Anxiety, a heightened state of arousal and negative affect, is an adaptive response essential for increasing awareness of potential threats in the environment. Research on the mechanisms leading to the pathological development of this response is crucial. The ventral tegmental area (VTA) is recognized as a key brain region for encoding information related to salient stimuli, and in recent years, has been attributed a novel role as a threat encoder and coordinator of defensive behaviors. The bed nucleus of the stria terminalis (BNST) actively mediates responses to uncertainty in the environment, and is at the interface between cognitive and autonomic systems to promote appropriate behavioral strategies. BNST dysfunction may, thus, lead to a sustained state of hypervigilance to unpredictability, a hallmark of anxiety disorders. In this work, we investigated the functional role of the VTA as an upstream regulator of BNST activity, combining anatomical, functional, and behavioral approaches. We hypothesized that VTA neuronal transmission in the BNST promotes innate defensive behaviors related to uncertainty, with an exacerbated co-activity generating anxious behavior. Our results demonstrate that distinct VTA cell subtypes project directly to multiple BNST subdivisions, establishing a functional connection by exciting BNST cell populations. This excitation translates into cell-type specific behaviors upon optical manipulation, including rewarding and anxiety-like behaviors. Further in vivo exploration of this microcircuit will enable us to elucidate its role in the development and maintenance of anxiety-like states.