The versatility and universality of Ca²⁺ signals stem from the breadth of their spatial and temporal dynamics. Spatially, Ca²⁺ signalling is well studied in the microdomain scale, close to a Ca²⁺ channel, and at the whole-cell level. However, little is known about how local Ca²⁺ signals are regulated to specifically activate spatially distant effectors without a global Ca²⁺ rise. Here we show that an intricate coupling between the inositol 1,4,5 trisphosphate (IP₃) receptor, SERCA pump and store-operated Ca²⁺ entry (SOCE) allows for efficient mid-range Ca²⁺ signalling. Ca²⁺ flowing through SOCE is taken up into the ER lumen by the SERCA pump, only to be re-released by IP₃Rs to activate distal Ca²⁺-activated Cl⁻ channels (CaCCs). This CaCC regulation contributes to setting the membrane potential of the cell. Hence functional coupling between SOCE, SERCA and IP₃R limits local Ca²⁺ diffusion and funnels Ca²⁺ through the ER lumen to activate a spatially separate Ca²⁺ effector.