Inhibitory synaptic plasticity is important for shaping both neuronal excitability and network activity. Here we investigate the input and GABA_A receptor subunit specificity of inhibitory synaptic plasticity by studying cerebellar interneuron–Purkinje cell (PC) synapses. Depolarizing PCs initiated a long-lasting increase in GABA-mediated synaptic currents. By stimulating individual interneurons, this plasticity was observed at somatodendritic basket cell synapses, but not at distal dendritic stellate cell synapses. Basket cell synapses predominantly express β2-subunit-containing GABA_A receptors; deletion of the β2-subunit ablates this plasticity, demonstrating its reliance on GABA_A receptor subunit composition. The increase in synaptic currents is dependent upon an increase in newly synthesized cell surface synaptic GABA_A receptors and is abolished by preventing CaMKII phosphorylation of GABA_A receptors. Our results reveal a novel GABA_A receptor subunit- and input-specific form of inhibitory synaptic plasticity that regulates the temporal firing pattern of the principal output cells of the cerebellum.