Apoptosis in most cell types is accompanied by altered Ca2+ homeostasis. During apoptosis, caspase‐3 mediated cleavage of the type 1 inositol 1,4,5‐trisphosphate receptor (IP3R1) generates a 95‐kDa C‐terminal fragment (C‐IP3R1), which represents the channel domain of the receptor. Aged mouse eggs display abnormal Ca2+ homeostasis and express C‐IP3R1, although whether or not C‐IP3R1 expression contributes to Ca2+ misregulation or a decrease in developmental competency is unknown. We sought to answer these questions by injecting in mouse oocytes and eggs cRNAs encoding C‐IP3R1. We found that: (1) expression of C‐IP3R1 in eggs lowered the Ca2+ content of the endoplasmic reticulum (ER), although, as C‐IP3R1 is quickly degraded at this stage, its expression did not impair pre‐implantation embryo development; (2) expression of C‐IP3R1 in eggs enhanced fragmentation associated with aging; (3) endogenous IP3R1 is required for aging associated apoptosis, as its down‐regulation prevented fragmentation, and expression of C‐IP3R1 in eggs with downregulated IP3R1 partly restored fragmentation; (4) C‐IP3R1 expression in GV oocytes resulted in persistent levels of protein, which abolished the increase in the ER releasable Ca2+ pool that occurs during maturation, undermined the Ca2+ oscillatory ability of matured eggs and their activation potential. Collectively, this study supports a role for IP3R1 and C‐IP3R1 in regulating Ca2+ homeostasis and the ER Ca2+ content during oocyte maturation. Nevertheless, the role of C‐IP3R1 on Ca2+ homeostasis in aged eggs seems minor, as in MII eggs the majority of endogenous IP3R1 remains intact and C‐IP3R1 undergoes rapid turnover. J. Cell. Physiol. © 2014 Wiley Periodicals, Inc.