Persistent inflammation is associated with a shift in spinal GABA_A signaling from inhibition to excitation such that GABA_A-receptor activation contributes to inflammatory hyperalgesia. We tested the hypothesis that the primary afferent is the site of the persistent inflammation-induced shift in GABA_A signaling which is due to a Na⁺–K⁺–Cl⁻-co-transporter (NKCC1)-dependent depolarization of the GABA_A current equilibrium potential (E_GABA). Acutely dissociated retrogradely labeled cutaneous dorsal root ganglion (DRG) neurons from naïve and inflamed (3days after a subcutaneous injection of complete Freund’s adjuvant) adult male rats were studied with Ca²⁺ imaging, western blot and gramicidin-perforated patch recording. GABA evoked a Ca²⁺ transient in a subpopulation of small- to medium-diameter capsaicin-sensitive cutaneous neurons. Inflammation was associated with a significant increase in the magnitude of GABA-induced depolarization as well as the percentage of neurons in which GABA evoked a Ca²⁺ transient. There was no detectable change in NKCC1 protein or phosphoprotein at the whole ganglia level. Furthermore, the increase in excitatory response was comparable in both HEPES- and HCO₃^--buffered solutions, but was only associated with a depolarization of E_GABA in HCO₃^--based solution. In contrast, under both recording conditions, the excitatory response was associated with an increase in GABA_A current density, a decrease in low threshold K⁺ current density, and resting membrane potential depolarization. Our results suggest that increasing K⁺ conductance in afferents innervating a site of persistent inflammation may have greater efficacy in the inhibition of inflammatory hyperalgesia than attempting to drive a hyperpolarizing shift in E_GABA.