Survival critically depends on the ability to detect threatening situations and in further selecting appropriate defensive behavior. This crucial mechanism contributed by contextual discrimination largely depends on the continuous evaluation of sensory cues that define the context. However, it may give rise to anxiety-related psychological disorders in situations of inaccurate context processing. We here aim to characterize neuronal determinants that allow the encoding and consolidation of contextual fear memory to successfully drive behavioral adaption, and mechanisms that especially induce context generalization, with particular emphasis on the contribution of exploratory/non-exploratory amygdala neurons ensembles in this process and their control by incoming hippocampal inputs.We thereby performed multisite extracellular recordings during online/offline states within the dorso-medial prefrontal cortex (dmPFC), basolateral amygdala (BLA) and ventral hippocampus (vHPC) networks and assessed their role along different steps of learning.We first showed that offline vHPC ripples are potent endogenous inputs for cortical/subcortical region reactivation, probably reflecting monosynaptic inputs and local neuronal connectivity. When assessed along the fear learning, the degree of BLA (but not dmPFC) activation by hippocampal ripples strongly reflected contextual fear generalization. Interestingly, hippocampal input distributions over exploratory/non-exploratory BLA ensembles were predictive of the future animal fear behaviors after conditioning. Further, strong hippocampal inputs were maintained in BLA neurons activated in the safe context for animals showing fear generalization, whereas progressively decreasing in other groups. Altogether, our results suggest that the targeting and refinement of hippocampal inputs onto BLA exploratory/non-exploratory ensembles is a key presynaptic determinant for contextual fear learning and generalization.