Stress can have profound consequences on mental health. While much is known about the neural circuits supporting associative memories of stressful events, our understanding of the circuits underlying the non-associative impacts of stress, such as heightened stress sensitivity and anxiety-related behavior, is limited. Here, we demonstrate that the ventral hippocampus (vHC) and basolateral amygdala (BLA) support distinct non-associative behavioral changes following stress. Inhibiting stress-induced protein synthesis in the BLA blocked subsequent increases in stress sensitivity but not anxiety-related behaviors. Conversely, inhibiting stress-induced protein synthesis in the vHC blocked subsequent increases in anxiety-related behavior but not stress sensitivity. Inhibiting neuronal activity in the BLA and vHC during the assessment of stress sensitivity or anxiety-related behavior recapitulated these structures' dissociable contributions to defensive behavior. Lastly, blocking the associative memory of a stressor had no impact on stress-induced changes in anxiety-related behavior. These findings highlight that multiple memory systems support the long-lasting effects of stress.