Memory is a one of the most fundamental capacities of the brain. In addition to providing a repository for recent experiences, memory supports a wide range of cognitive functions including navigation, imagination, and sensory perception. While some facets of memory are well understood, including the essential role that the hippocampus plays in many forms of learning and the importance of neocortical regions for long-term memory storage, a complete mechanistic explanation for how memory supports cognition remains out of reach. A major obstacle is a lack of research into the form and development of neocortical memory representations, and how they participate in cognitive processes. To therefore provide insight into the role that neocortical regions play in memory, I examined the activity of large populations of neurons in the retrosplenial cortex (RSC) in awake, behaving rats as they performed spatial navigation tasks. The RSC is active during many memory-based cognitive functions in both humans and rats, and lesions of the RSC cause multiple forms of amnesia, including an inability to navigate. I find that neuronal activity patterns in the RSC form rich representations of two of the most important components of memory: space and time. I demonstrate that spatial representations develop slowly in the RSC over the course of many experiences, and that these representations are particularly sensitive to the spatial arrangement of the environment. I also found that the moment-to-moment nature of these representations correlates with the rat’s navigational proficiency, and that they can be used to predict the rat’s future navigation behaviors, including upcoming memory failures. Lastly, I show that the activity of RSC ensembles selectively represents the rat’s future goal location during instances when the rat must select between multiple destinations. Thus, my research provides support for the idea that neocortical memory regions support cognition through the reactivation of long-term memory representations relevant to the current behavior.