H⁺ ions are powerful modulators of cardiac function, liberated during metabolic activity. Among their physiological effects is a chemical gating of cell-to-cell communication, caused by H⁺-mediated closure of connexin (Cx) channels at gap junctions. This protects surrounding tissue from the damaging effects of local intracellular acidosis. Cx proteins (largely Cx-43 in ventricle) form multimeric pores between cells, permitting translocation of ions and other solutes up to 1 kDa. The channels are essential for electrical and metabolic coordination of a tissue. Here we demonstrate that, contrary to expectation, H⁺ ions can induce an increase of gap-junctional permeability. This occurs during modest intracellular acid loads in myocyte pairs isolated from mammalian ventricle. We show that the increase in permeability allows a local rise of [H⁺]_i to dissipate into neighboring myocytes, thereby providing a mechanism for spatially regulating intracellular pH (pH_i). During larger acid loads, the increased permeability is overridden by a more familiar H⁺-dependent inhibition (H⁺ inactivation). This restricts cell-to-cell H⁺ movement, while allowing membrane H⁺ transporters such as Na⁺/H⁺ exchange, to extrude the acid from the cell. The H⁺ sensitivity of Cx channels therefore defines whether junctional or sarcolemmal mechanisms are selected locally for the removal of an acid load. The bell-shaped pH dependence of permeability suggests that, in addition to H⁺ inactivation, an H⁺-activation process regulates the ensemble of Cx channels open at the junction. As well as promoting spatial pH_i regulation, H⁺ activation of junctional permeability may link increased metabolic activity to improved myocardial coupling, the better to meet mechanical demand.