Phosphorylation of BCL‐2 within an unstructured loop inhibits its antiapoptotic effect. We found that phosphorylated BCL‐2 predominantly localized to the endoplasmic reticulum (ER) and tested whether phosphorylation would control its activity at this organelle, where Ca²⁺ dynamics serve as a critical control point for apoptosis. Phosphorylation greatly inhibits the ability of BCL‐2 to lower [Ca²⁺]_er and protect against Ca²⁺‐dependent death stimuli. Cells expressing nonphosphorylatable BCL‐2^AAA exhibited increased leak of Ca²⁺ from the ER and further diminished steady‐state [Ca²⁺]_er stores when compared to cells expressing BCL‐2^wt. Consequently, when BCL‐2 is phosphorylated, Ca²⁺ discharge from the ER is increased, with a secondary increase in mitochondrial Ca²⁺ uptake. We also demonstrate that phosphorylation of BCL‐2 inhibits its binding to proapoptotic family members. This inhibitory mechanism manifested at the ER, where phosphorylated BCL‐2 was unable to bind proapoptotic members. [Ca²⁺]_er proved coordinate with the capacity of BCL‐2 to bind proapoptotic BH3‐only members, further integrating the apoptotic pathway and Ca²⁺ modulation. Unexpectedly, the regulation of ER Ca²⁺ dynamics is a principal avenue whereby BCL‐2 phosphorylation alters susceptibility to apoptosis.