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The temperature dependence of miniature endplate current (MEPC) amplitude (Ac), 20–80% rise time (tr), and 90–33% fall-time (tf) was determined for lizard (Anolis carolinensis) intercostal muscle using broadband extracellular (EC) and voltage clamp (VC) recordings. Voltage clamp methods were optimized for the fast MEPC rising phase using custom electronics. From 0–43°C, Ac increased by ∼4.2-fold, while tr and tf decreased by ∼3.6- and ∼9.5-fold, respectively. Arrhenius plots were smoothly curved, with small apparent Q10 (Ac) or (Q10)−1 (tr and tf) values mostly well below 2.0. Nearly identical extracellular and voltage clamp results ruled out measurement artifacts, even for the shortest tr values (<60μs). Monte Carlo simulation of MEPCs showed that a single underlying rate cannot determine the observed temperature dependence. To quantitatively reproduce the experimental tf results, a minimal model required activation energies of 46.0 (Q10∼2.0) and 63.6 (Q10∼2.5) kJ mol−1 for channel opening and closing, respectively, and accounted for most of the observed changes in Ac and tr as well. Thus, relatively large but offsetting temperature sensitivities of channel gating mostly govern and minimize the temperature dependence of MEPCs, preserving the safety factor for neuromuscular transmission. Additional temperature-sensitive parameters that could fine-tune the minimal model are discussed.