Key points Short‐term facilitation takes place at GABAergic synapses between cerebellar Purkinje cells (PCs). By directly patch clamp recording from a PC axon terminal, we studied the mechanism of short‐term facilitation. We show that the Ca2+ currents elicited by high‐frequency action potentials were augmented in a [Ca2+]i‐dependent manner. The facilitation of synaptic transmission showed 4–5th power dependence on the Ca2+ current facilitation, and was abolished when the Ca2+ current amplitude was adjusted to be identical. Short‐term facilitation of Ca2+ currents predominantly mediates short‐term facilitation at synapses between PCs. Abstract Short‐term synaptic facilitation is critical for information processing of neuronal circuits. Several Ca2+‐dependent positive regulations of transmitter release have been suggested as candidate mechanisms underlying facilitation. However, the small sizes of presynaptic terminals have hindered the biophysical study of short‐term facilitation. In the present study, by directly recording from the axon terminal of a rat cerebellar Purkinje cell (PC) in culture, we demonstrate a crucial role of [Ca2+]i‐dependent facilitation of Ca2+ currents in short‐term facilitation at inhibitory PC–PC synapses. Voltage clamp recording was performed from a PC axon terminal visualized by enhanced green fluorescent protein, and the Ca2+ currents elicited by the voltage command consisting of action potential waveforms were recorded. The amplitude of presynaptic Ca2+ current was augmented upon high‐frequency paired‐pulse stimulation in a [Ca2+]i‐dependent manner, leading to paired‐pulse facilitation of Ca2+ currents. Paired recordings from a presynaptic PC axon terminal and a postsynaptic PC soma demonstrated that the paired‐pulse facilitation of inhibitory synaptic transmission between PCs showed 4–5th power dependence on that of Ca2+ currents, and was completely abolished when the Ca2+ current amplitude was adjusted to be identical. Thus, short‐term facilitation of Ca2+ currents predominantly mediates short‐term synaptic facilitation at synapses between PCs.