Being able to flexibly remember aversive events is a critical neural function for mammals. However, aversive memories can have a negative impact on animal well-being if they are not restricted to the appropriate context, or not updated with new information over time. The hippocampus is a key brain region for both forming and updating aversive memories –specifically, the dorsal section of hippocampal area CA1 is crucial for integrating spatial and non-spatial information into coherent contextual memories. My doctoral work focuses on understanding the hippocampal circuits underlying the formation, recall, and extinction of aversive memories. In Chapter 2, I reveal the contextual fear-suppressive role of the projection from the thalamic subregion nucleus reuniens (NR) to dorsal CA1. I implemented a novel head-restrained virtual reality contextual fear conditioning paradigm (VR-CFC) where I administered mild tail shocks in one context (shocked) but not the other (neutral). I showed that inactivation of the NR-CA1 pathway following VR-CFC increases fearful freezing, induces fear generalization to a neutral context, and delays extinction of fearful responses. Using in vivo sub-cellular calcium imaging, I found that NR-axons become selectively tuned to fearful freezing only after VR-CFC. In Chapter 3, I demonstrate how the NR-CA1 pathway impacts population dynamics in excitatory pyramidal neuron somata in dorsal CA1 throughout VR-CFC. I reveal that with the NR-CA1 pathway intact, CA1 somata are preferentially active in the shocked context after shocks, globally remap their place fields to more flexible post-fear extinction maps, tune to both shocks and to freezing epochs, and increase both the frequency and scale of simultaneous neural activations. In contrast, I show that inhibiting the NR-CA1 pathway prevents preferential activity in the shocked context post-shocks by over-activating somata, interferes with global remapping by retaining more stable post-extinction maps, increases freeze-tuning, and disrupts simultaneous neural activations. Lastly, in Chapter 4, I investigated the differential activity of the basal and apical dendritic arbors through novelty and reward manipulation. I reveal functional segregation between predominantly spatial representations in the basal dendrites and predominantly non-spatial reward and novelty-modulated representations in the apical dendrites, paving the way for future investigations of dendritic mechanisms underlying somatic activity changes in VR-CFC. Overall, this dissertation provides both methodological and experimental leaps forward in our understanding of how the hippocampus flexibly encodes aversive experiences by highlighting the critical role of projections from thalamic nucleus reuniens to hippocampal dorsal CA1. I pioneered a novel contextual fear conditioning paradigm in virtual reality that reliably elicits context-dependent freezing behaviors similar to non-head-fixed behavior. I imaged two distal subcellular components for the first time – NR axons and dorsal CA1 distal apical tuft dendrites – and developed a new technique for identifying population-level synchronized activity in dorsal CA1 somata. Our findings paint a picture of hippocampal dorsal CA1 as a critical region for memory that both encodes a variety of salient features to aversive contextual memories and flexibly updates fear memories to extinguish fear responses through modulating inputs from thalamic nucleus reuniens.