Cerebellar neurones show complex and differentiated mechanisms of action potential generation that have been proposed to depend on peculiar properties of their voltage‐dependent Na⁺ currents. In this study we analysed voltage‐dependent Na⁺ currents of rat cerebellar granule cells (GCs) by performing whole‐cell, patch‐clamp experiments in acute rat cerebellar slices. A transient Na⁺ current (I_NaT) was always present and had the properties of a typical fast‐activating/inactivating Na⁺ current. In addition to I_NaT, robust persistent (I_NaP) and resurgent (I_NaR) Na⁺ currents were observed. I_NaP peaked at ∼−40 mV, showed half‐maximal activation at ∼−55 mV, and its maximal amplitude was about 1.5% of that of I_NaT. I_NaR was elicited by repolarizing pulses applied following step depolarizations able to activate/inactivate I_NaT, and showed voltage‐ and time‐dependent activation and voltage‐dependent decay kinetics. The conductance underlying I_NaR showed a bell‐shaped voltage dependence, with peak at −35 mV. A significant correlation was found between GC I_NaR and I_NaT peak amplitudes; however, GCs expressing I_NaT of similar size showed marked variability in terms of I_NaR amplitude, and in a fraction of cells I_NaR was undetectable. I_NaT, I_NaP and I_NaR could be accounted for by a 13‐state kinetic scheme comprising closed, open, inactivated and blocked states. Current‐clamp experiments carried out to identify possible functional correlates of I_NaP and/or I_NaR revealed that in GCs single action potentials were followed by depolarizing afterpotentials (DAPs). In a majority of cells, DAPs showed properties consistent with I_NaR playing a role in their generation. Computer modelling showed that I_NaR promotes DAP generation and enhances high‐frequency firing, whereas I_NaP boosts near‐threshold firing activity. Our findings suggest that special properties of voltage‐dependent Na⁺ currents provides GCs with mechanisms suitable for shaping activity patterns, with potentially important consequences for cerebellar information transfer and computation.