Small dorsal root ganglion neurons express preferentially the Na⁺ channel isoform Na_V1.9 that mediates a tetrodotoxin-resistant (TTX-R) Na⁺ current. We investigated properties of the Na⁺ current mediated by Na_V1.9 (I_NaN) using the whole-cell, patch-clamp recording technique. To isolate I_NaN from heterogeneous TTX-R Na⁺ currents that also contain another type of TTX-R Na⁺ current mediated by Na_V1.8, we used Na_V1.8-null mutant mice. When F⁻ was used as an internal anion in the patch pipette solution, both the activation and inactivation kinetics for I_NaN shifted in the hyperpolarizing direction with time. Such a time-dependent shift of the kinetics was not observed when Cl⁻ was used as an internal anion. Functional expression of I_NaN declined with time after cell dissociation and recovered during culture, implying that Na_V1.9 may be regulated dynamically by trophic factors or depend on subtle environmental factors for its survival. During whole-cell recordings, the peak amplitude of I_NaN increased dramatically after a variable delay, as if inactive or silent channels had been “kindled”. Such an unusual increase of the amplitude could be prevented by adding ATP to the pipette solution or by recording with the nystatin-perforated patch-clamp technique, suggesting that the rupture of patch membrane affected the behaviour of Na_V1.9. These peculiar properties of I_NaN may provide an insight into the plasticity of Na⁺ channels that are related to pathological functions of Na⁺ channels accompanying abnormal pain states.