The neural basis underlying the relationship between a contextual memory and its constituent features is not well understood; in particular, where features are represented in the brain and how they drive memory recall. To gain insight into this question, we developed a behavioral task where mice use features to recall an associated contextual memory. We performed longitudinal imaging in hippocampus as mice performed this task and identified robust representations of global context. To identify putative brain regions that provide feature inputs to the hippocampus, we inhibited cortical afferents while imaging hippocampus during behavior. We found that while inhibition of entorhinal inputs led to broad silencing of hippocampus, inhibition of prefrontal anterior cingulate inputs led to a highly specific silencing of context neurons and deficits in feature-based recall. Single neurons in AC displayed feature-selectivity as well as mixed-selectivity to combinations of features, in contrast to the strong conjunctive tuning that was observed with CA1 neurons. These multiplexed single neuron activities gave rise to robust population level representations of features. Interestingly, we observed that AC feature representations 1) lag hippocampus context representations during training, but 2) dynamically reorganize to lead and target recruitment of context ensembles in hippocampus during recall. This AC-CA1 interaction is further enhanced by the saliency of the memory, as suggested by tight coupling of feature-context ensembles in reinforced compared to non-reinforced contexts. Together, we provide neurophysiological insights into how feature representations emerge, stabilize, and access long-range episodic representations to drive memory recall.