Atrial fibrillation (AF) is characterized by sustained high atrial activation rates and arrhythmogenic cellular Ca²⁺ signaling instability; however, it is not clear how a high atrial rate and Ca²⁺ instability may be related. Here, we characterized subcellular Ca²⁺ 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 Ca²⁺ signaling. Ca²⁺ sparks, arrhythmogenic Ca²⁺ waves, sarcoplasmic reticulum (SR) Ca²⁺ leak, and SR Ca²⁺ content were largely unaltered. Based on computational analysis, these findings were consistent with a higher Ca²⁺ leak due to PKA-dependent phosphorylation of SR Ca²⁺ channels (RyR2s), fewer RyR2s, and smaller RyR2 clusters in the SR. We determined that less Ca²⁺ release per [Ca²⁺]_i transient, increased Ca²⁺ buffering strength, shortened action potentials, and reduced L-type Ca²⁺ 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 [Ca²⁺]_i signal to the myocyte center. We conclude that sustained high atrial rates alone silence Ca²⁺ signaling and do not produce Ca²⁺ signaling instability, consistent with an adaptive molecular and cellular response to atrial tachycardia.