Intestinal fluid secretion is driven by apical membrane, cystic fibrosis transmembrane conductance regulator (CFTR)‐mediated efflux of Cl– that is concentrated in cells by basolateral Na⁺−K⁺−2Cl– cotransporters (NKCC1). An absolute requirement for Cl– efflux is the parallel activation of K⁺ channels which maintain a membrane potential that sustains apical anion secretion. Both cAMP and Ca²⁺ are intracellular signals for intestinal Cl– secretion. The K⁺ channel involved in cAMP‐dependent secretion has been identified as the KCNQ1–KCNE3 complex, but the identity of the K⁺ channel driving Ca²⁺‐activated Cl– secretion is controversial. We have now used a Kcnn4 null mouse to show that the intermediate conductance IK1 K⁺ channel is necessary and sufficient to support Ca²⁺‐dependent Cl– secretion in large and small intestine. Ussing chambers were used to monitor transepithelial potential, resistance and equivalent short‐circuit current in colon and jejunum from control and Kcnn4 null mice. Na⁺, K⁺ and water content of stools was also measured. Distal colon and small intestinal epithelia from Kcnn4 null mice had normal cAMP‐dependent Cl– secretory responses. In contrast, they completely lacked Cl– secretion in response to Ca²⁺‐mobilizing agonists. Ca²⁺‐activated electrogenic K⁺ secretion was increased in colon epithelium of mice deficient in the IK1 channel. Na⁺ and water content of stools was diminished in IK1‐null animals. The use of Kcnn4 null mice has allowed us to demonstrate that IK1 K⁺ channels are solely responsible for driving intestinal Ca²⁺‐activated Cl– secretion. The absence of this channel leads to a marked reduction in water content in the stools, probably as a consequence of decreased electrolyte and water secretion.