Memories associating personal experiences and places can be recalled after extended periods of life-time. Despite the current prevailing view that episodic memories are fully allocated to cortical areas after an initial encoding phase within the hippocampus, lesion studies suggest that memories might be partially retained within the hippocampus. We hypothesize that sparsely active and spatially tuned dentate gyrus granule cell (GC) assemblies efficiently store and retrieve episodic memories over extended live spans.We employed two-photon in vivo calcium-imaging of somata and mossy-fiber boutons of GCs in mice navigating through virtual environments to investigate formation, discrimination and recall of spatial memories. We show that formation and stabilization of GC assemblies representing novel environments emerged over 3-4 subsequent days. Increasing the number of daily exposures to a novel context did not overcome these slow dynamics. After formation, maps remained remarkably stable, with individual GCs maintaining their fields for ~90 days. Similarly, stable context-specific place-fields of mossy-fiber boutons could be recorded over ~10 days in familiar environments. To overcome the slow emergence, we chemogenetically excited GCs by activating hM3Dq-receptors during 5 days of novel context exploration. A substantial fraction of place cells emerged but despite their reactivation, most of them were not permanently integrated in the novel map. Indeed, formation of the final map took also ~3 days. Thus, GC place cells provide stable and context-specific outputs to downstream CA2/3, which seems to be robust against network perturbations. This ability might be an important requirement for long-term storage of spatial and contextual information.