A fundamental theoretical tension exists between the role of the hippocampus in generalizing across a set of related episodes, and in supporting memory for individual episodes. Whilst the former requires an appreciation of the commonalities across episodes, the latter emphasizes the representation of the specifics of individual experiences. We developed a novel version of the hippocampal-dependent paired associate inference (PAI) paradigm, which afforded us the unique opportunity to investigate the relationship between episodic memory and generalization in parallel. Across four experiments, we provide surprising evidence that the overlap between object pairs in the PAI paradigm results in a marked loss of episodic memory. Critically, however, we demonstrate that superior generalization ability was associated with stronger episodic memory. Through computational simulations we show that this striking profile of behavioral findings is best accounted for by a mechanism by which generalization occurs at the point of retrieval, through the recombination of related episodes on the fly. Taken together, our study offers new insights into the intricate relationship between episodic memory and generalization, and constrains theories of the mechanisms by which the hippocampus supports generalization.