Neurons are highly temperature sensitive. Temperature-induced nerve failure may play an important role in determining organismal thermal tolerance limits and distribution patterns. To expand our understanding of the role of neuronal thermal performance in setting thermal limits, we compared the thermal performance of neurons from five porcelain crab (genus Petrolisthes) congeners that differ in thermal habitat. In experiment 1, neuronal performance of sensory neurons was determined by extracellular recording of spontaneous action potentials during thermal ramps. Arrhenius break temperatures of action potential generation were used to calculate maximum critical temperature (CT(max)) and minimum critical temperature (CT(min)) for neuronal performance. CT(max) and CT(min) were related to habitat temperature across the five species and were found to respond to acclimation temperature. In experiment 2, we assessed the performance of neurons from Petrolisthes cinctipes acclimated at 8°, 18°, and 25°C when placed at 30°C (near the whole-organism CT(max) of this species) and demonstrated that neural performance near whole-organism CT(max) increases with increasing acclimation temperature. In experiment 3, we compared the thermal limits of sensory afferents and pacemaker efferents and found that they were correlated, although pacemaker efferents tended to have a higher CT(max) and reduced plasticity. Our final analysis, which was of transcriptomic data in cardiac tissue, leads us to hypothesize that nerve membrane K(+) conductance may underlie variation in nerve thermal tolerance.