Episodic memory involves the representation of memories shared across a global context as well as that of unique events that occurred within it. To examine how parahippocampal subregions support this balance, participants encountered multiple objects in each building of a virtual environment and later retrieved the building associated with each cued object during fMRI scanning. Across the MTL, objects from the same building showed greater representational similarity than those from different buildings, indicating integration of contextually associated memories. This effect was observed only for task-relevant contexts (i.e., buildings but not corners). Higher similarity in the EC and lower similarity in the PrC were associated with performance, and integration in the EC mediated the role of CA3DG in memory retrieval. These findings extend current computational models of how the MTL represents context-dependent memories and demonstrate the complementary and opposing roles of the PrC and EC in supporting memory integration and differentiation.