The hippocampal dentate gyrus (DG) to CA3 pathway plays a key role in encoding new experiences that are ultimately consolidated in the anterior cingulate cortex (ACC). Experience-dependent changes among excitatory neurons in the DG ‒ CA3 circuit have been intensely studied. However, DG cell axons innervate not only CA3 pyramidal neurons but also inhibitory, parvalbumin positive interneurons (PV IN) to provide strong feed-forward inhibition (FFI) onto CA3 pyramidal neurons. Following learning, FFI onto CA3 is temporarily increased which may be a key element for consolidation and long-term memory storage in hippocampal ‒ cortical networks1; 2. Computationally, feed-forward inhibition has been suggested to support spike-timing fidelity and regulate bursting activity. However, the underlying mechanisms through which this inhibitory microcircuit mediates memory consolidation in hippocampal ‒ cortical networks are not well understood. Here, we harnessed a molecular tool2 to investigate how increased FFI in this microcircuit affects downstream neuronal ensembles and network oscillations during memory consolidation. We performed longitudinal in vivo calcium imaging in CA1 and ACC during contextual fear learning in mice with virally enhanced FFI in the DG ‒ CA3 circuit. We found that selectively increasing FFI onto CA3 facilitated formation and maintenance of neuronal representation, in form of context-associated neuronal ensembles, in both brain regions as it prevented a time-dependent decay of neuronal representations. Furthermore, the specificity of neuronal ensembles was increased in a time-dependent manner in ACC. Simultaneous recordings of local field potentials (LFPs) in CA1 and ACC revealed that virally enhanced FFI in DG ‒ CA3 increased coupling of CA1 sharp-wave ripples and ACC spindles, a mechanism for hippocampal ‒ cortical communication during memory consolidation3. This study links a defined synaptic mechanism in a DG ‒ CA3 inhibitory microcircuit with ensemble dynamics and network oscillations and provides direct evidence for its role in memory consolidation.