Memories are believed to be encoded by sparse ensembles of neurons in the brain. Although individual memory traces are generally assumed to be functionally homogeneous entities, theoretical studies suggest that functional heterogeneity within each trace could be advantageous for efficient information encoding and flexible memory expression. In this study, we directly investigated the functional heterogeneity within contextual fear memory engrams in the mouse dentate gyrus (DG). We identified two neuronal ensembles, genetically defined by the Fos- or Npas4-dependent transcriptional pathways, which oppositely regulated the behavioral output of contextual fear memories. The Fos-dependent ensemble promotes memory generalization and receives enhanced excitatory synaptic inputs. On the contrary, theNpas4-dependent ensemble mediates memory discrimination and receives enhanced inhibitory synaptic drive. To demonstrate that activity-dependent pathways define the functionalities of neuronal ensembles within the engram, we showed that Npas4 regulated adaptive memory expression and inhibitory synaptic transmission, recapitulating the functions of the Npas4-dependent ensemble. Taken together, our findings support a working model in which distinct neuronal ensembles undergo different activity-dependent cellular and circuit changes after learning and, as a result, differentially drive memory-guided behaviors.