Interstitial cells of Cajal (ICC) act as pacemaker cells in the gastrointestinal tract by generating electrical slow waves to regulate rhythmic smooth muscle contractions. Intrinsic Ca²⁺ oscillations in ICC appear to produce the slow waves by activating pacemaker currents, currently thought to be carried by the Ca²⁺-activated Cl^- channel, anoctamin 1 (Ano1). In this paper we present a novel model of small intestinal ICC pacemaker activity that incorporates store-operated Ca²⁺ entry and a new model of Ano1 current. A series of simulations were carried out with the ICC model to investigate current controversies about the reversal potential of the Ano1 Cl^- current in ICC, and to predict the characteristics of the other ion channels that are necessary to generate slow waves. The model results show that Ano1 is a plausible pacemaker channel when coupled to a store-operated Ca²⁺ channel, but suggest that small cyclical depolarizations may still occur in ICC in Ano1 knockout mice. The results predict that voltage-dependent Ca²⁺ current is likely to be negligible during the slow wave plateau phase. The model shows that the Cl^- equilibrium potential is an important modulator of slow wave morphology, highlighting the need for a better understanding of Cl^- dynamics in ICC.