Parvalbumin-positive interneurons (PVIs) in the dentate gyrus (DG) possess dendritic spines, but their functional properties and structural dynamics remain uncharted. Using in vitro 2-Photon imaging, we show that glutamatergic synapses at PVI dendritic spines evoke AMPA and NMDA receptor-mediated calcium signals with high spatial compartmentalization defined by their neck length. Ex vivo morphological analysis shows that DREADD-mediated in vivo PVI excitation increases spine density and length, whereas recruitment of glutamatergic inputs causes spine head enlargement. These spine dynamics could be reproduced in mice experiencing novel contexts. By using dual-eGRASP-mediated input labeling we provide evidence that experience-driven PVI spine growth and input density boosts synaptic targeting of PVI spines over shafts, a mechanism supporting functional isolation of postsynaptic signals from parent dendrites. We propose that experience-related PVI spine dynamics echo excitation levels of the DG network allowing PVIs to dynamically adjust their microcircuit integration in relation to the networks’ computational demands.