Neuronal networks require precise coordination of excitatory and inhibitory synaptic connectivity to function properly. Regulation of parvalbumin-positive (PV+) interneuron activity is especially important for network function, and changes in PV+ interneuron activity correlate with an animal’s performance in learning tasks. Previously, changes in PV+ interneuron connectivity have been shown to regulate excitatory pyramidal cell activity. However, the mechanism via which PV+ interneurons control their own activity remains unknown. Here we used a chemogenetic approach to change the activity of PV+ interneurons and performed whole-cell electrophysiological recordings to assess compensatory changes in the excitatory and inhibitory inputs they receive. We find that increasing or decreasing the activity of PV+ interneuron activity specifically leads to a cell-autonomous compensatory change in inhibitory, but not excitatory, synaptic connectivity. Further optogenetic experiments revealed that these synaptic changes originate exclusively from other PV+ interneurons. We next performed ribosome profiling experiments to identify the molecular mechanisms mediating the activity-dependent scaling of PV+ synapses onto PV+ interneurons. To this end, we combined chemogenetics with viral Translating Ribosome Affinity Purification (vTRAP) to isolate mRNAs that are specifically translated in activated PV+ interneurons. Subsequent RNA-sequencing revealed that increasing the activity of PV+ interneurons leads to the cell-autonomous upregulation of two genes encoding multiple secreted neuropeptides, Vgf and Scg2. Functional experiments demonstrated that VGF is critically required for the activity-dependent scaling of inhibitory PV+ synapses onto PV+ interneurons. Our findings reveal an instructive role for neuropeptide-encoding genes in regulating synaptic connections among PV+ interneurons.