Atrial fibrillation (AF) is characterized by sustained high atrial activation rates and arrhythmogenic cellular Ca signaling instability; however, it is not clear how a high atrial rate and Ca instability may be related. Here, we characterized subcellular Ca signaling after 5 days of high atrial rates in a rabbit model. While some changes were similar to those in persistent AF, we identified a distinct pattern of stabilized subcellular Ca signaling. Ca sparks, arrhythmogenic Ca waves, sarcoplasmic reticulum (SR) Ca leak, and SR Ca content were largely unaltered. Based on computational analysis, these findings were consistent with a higher Ca leak due to PKA-dependent phosphorylation of SR Ca channels (RyR2s), fewer RyR2s, and smaller RyR2 clusters in the SR. We determined that less Ca release per [Ca]i transient, increased Ca buffering strength, shortened action potentials, and reduced L-type Ca current contribute to a stunning reduction of intracellular Na concentration following rapid atrial pacing. In both patients with AF and in our rabbit model, this silencing led to failed propagation of the [Ca]i signal to the myocyte center. We conclude that sustained high atrial rates alone silence Ca signaling and do not produce Ca signaling instability, consistent with an adaptive molecular and cellular response to atrial tachycardia.