Atrial fibrillation (AF) is characterized by sustained high atrial activation rates and cellular Ca2+ signaling instability, which is thought to contribute to atrial arrhythmogenesis. How high rate and arrhythmogenic Ca2+ instability may be related, however, is poorly understood. We have characterized the effect of sustained high atrial activation rates on sub-cellular Ca2+ signaling in a rabbit model. L-type Ca2+ current and whole cell [Ca2+]i transient were reduced as was ryanodine receptor (RyR2) expression (by 77%) with a 7fold increase in RyR2 phosphorylation (Ser2809). Ca2+ release in the myocyte center was blunted due to increased [Ca2+] buffering strength. The spatial distribution of junctional and central SR sites was unchanged. Surprisingly, SR Ca2+ content, characteristics and rates of Ca2+ sparks and -waves were unchanged. Computational estimates of Ca2+ signaling suggest that the observed behavior arises from a higher Ca2+ leak rate per RyR2 associated with less RyR2s per SR cluster. Additionally, lower total Ca2+ release per [Ca2+]i transient, due to failed Ca2+ wave propagation to the myocyte center and the higher Ca2+ buffering strength contribute. Sustained high atrial rates produce “Ca2+ signaling silencing” and not Ca2+ instability. Ca2+ signaling silencing serves as an adaptive response to rapid myocyte activation and this hampers the development of Ca2+ dysregulation-based arrhythmogenic mechanisms