ICC generate electrical slow waves by coordinated openings of ANO1 channels, a Ca²⁺-activated Cl^- (CaCC) conductance. Efflux of Cl^- during slow waves must be significant as there is high current density during slow wave currents and slow waves are of sufficient magnitude to depolarize the syncytium of smooth muscle cells and PDGFRα⁺ cells to which they are electrically coupled. We investigated how the driving force for Cl^- current is maintained in ICC. We found robust expression of Slc12a2 (which encodes a Na⁺K⁺Cl^- cotransporter, NKCC1) and immunohistochemical confirmation that NKCC1 is expressed in ICC. Using the gramicidin permeabilized-patch technique, which is reported to not disturb [Cl^-]_i, the reversal potential for spontaneous transient inward currents (E_STICs) was -10.5 mV. This value corresponds to the peak of slow waves when they are recorded directly from ICC in situ. Inhibition of NKCC1 with bumetanide shifted E_STICs to more negative potentials within a few minutes and reduced pacemaker activity. Bumetanide had no direct effects on ANO1 or Ca_V3.2 channels expressed in HEK 293 cells, or L-type Ca²⁺ currents. Reducing extracellular Cl^- to 10 mM shifted E_STICs to positive potentials as predicted by the Nernst equation. The relatively rapid shift in E_STICs when NKCC1 was blocked suggests that significant changes in the transmembrane Cl^- gradient occur during the slow wave cycle, possibly within microdomains formed between ER and the plasma membrane in ICC. Recovery of Cl^- via NKCC1 might have additional consequences on shaping the waveforms of slow waves via Na⁺ entry into microdomains.