In cardiac excitation‐contraction coupling, Ca²⁺‐induced Ca²⁺ release (CICR) from ryanodine receptors (RyRs), triggered by Ca²⁺ entry through the nearby L‐type Ca²⁺ channel, induces Ca²⁺‐dependent inactivation (CDI) of the Ca²⁺ channel. Aiming at elucidating the physiological role of CDI produced by CICR (CICR‐dependent CDI), we investigated the contribution of the CICR‐dependent CDI to action potential (AP) waveform and the amount of Ca²⁺‐influx through Ca²⁺ channels during AP in rat ventricular myocytes. The elimination of the CICR‐dependent CDI, by depletion of the SR Ca²⁺ with thapsigargin, significantly prolonged AP duration (APD). APD changed in parallel with the magnitude of CICR during the recovery of the SR Ca²⁺ content after transient depletion by caffeine. Such CICR‐dependent change of APD persisted under the highly Ca²⁺ buffered condition where the Ca²⁺ signalling was restricted to nanoscale domains. Blockers of the Ca²⁺‐dependent Cl⁻ channel or the BK channel did not affect AP waveform. The amount of Ca²⁺‐influx through Ca²⁺ channels during the SR‐depleted type AP waveform, measured in the SR‐depleted myocyte, was increased by 40% over that during the SR‐intact type AP waveform measured in the SR‐intact myocyte. The protein kinase A stimulation further enhanced the Ca²⁺‐influx during AP under the SR‐depleted condition to 70% of that under the SR‐intact condition. These results indicate that the CICR‐dependent CDI of L‐type Ca²⁺ channels, under control of the privileged cross‐signalling between L‐type Ca²⁺ channels and RyRs, play important roles for monitoring and tuning the SR Ca²⁺ content via changes of AP waveform and the amount of Ca²⁺‐influx during AP in ventricular myocytes.