MiRP3, the single‐span membrane protein encoded by KCNE4, is localized by immunofluorescence microscopy to the transverse tubules of murine cardiac myocytes. MiRP3 is found to co‐localize with Kv4.2 subunits that contribute to cardiac transient outward potassium currents (Ito). Whole‐cell, voltage‐clamp recordings of human MiRP3 and Kv4.2 expressed in a clonal cell line (tsA201) reveal MiRP3 to modulate Kv4.2 current activation, inactivation and recovery from inactivation. MiRP3 shifts the half‐maximal voltage for activation (V1/2) ∼20 mV and slows time to peak ∼100%. In addition, MiRP3 slows inactivation ∼100%, speeds recovery from inactivation ∼30%, and enhances restored currents so they ‘overshoot’ baseline levels. The cytoplasmic accessory subunit KChIP2 also assembles with Kv4.2 in tsA201 cells to increase peak current, shift V1/2∼5 mV, slow time to peak ∼10%, slow inactivation ∼100%, and speed recovery from inactivation ∼250% without overshoot. Simultaneous expression of all three subunits yields a biophysical profile unlike either accessory subunit alone, abolishes MiRP3‐induced overshoot, and allows biochemical isolation of the ternary complex. Thus, regional heterogeneity in cardiac expression of MiRP3, Kv4.2 and KChIP2 in health and disease may establish the local attributes and magnitude of cardiac Ito.