Intracellular Ca2+ oscillations are made of highly spatially and timely controlled cytoplasmic waves of Ca2+ fueled by two main Ca2+ sources: the extracellular compartment and the endoplasmic reticulum (ER). Specific and highly regulated ion channels and pumps located at the plasma and ER membranes control the cytoplasmic Ca2+ levels as well as ER store refilling. When ER Ca2+ stores are depleted a mechanism termed Store-Operated Calcium Entry (SOCE) drives Ca2+ entry. In the oocyte of the frog Xenopus laevis intracellular Ca2+ variations are converted into chloride currents by Ca2+-Activated Chloride Channels (CACC) allowing real time monitoring of sub-plasma membrane Ca2+ levels. We recently showed that SOCE and IP3 receptors (IP3R) define a functional complex creating mid-range Ca2+ signaling to CACC (Courjaret and Machaca, 2014). Here we aimed at understanding how SOCE influences intracellular Ca2+ release by IP3R and Ca2+ oscillations. Injecting a non-hydrolysable IP3 analog induced transient Ca2+ oscillation (≈20 min) and stimulated SOCE. When Ca2+ influx through SOCE was increased by hyperpolarizing pulses or reduced by removing extracellular Ca2+, the duration of the Ca2+ oscillations was respectively reduced or increased. In addition, removing extracellular Ca2+ more than 30 minutes after the end of the oscillation restored the Ca2+ release, indicating that the emptying of the ER stores cannot account for the inhibition of Ca2+ oscillations. It was also possible to trigger Ca2+ release events after the end of the Ca2+ oscillations by inducing a large SOCE. Those events precisely depend on the amplitude and timing of SOCE. Imaging of intracellular Ca2+ also revealed that they only occur at the animal pole of the oocyte, where SOCE is larger. This indicates that a strong reloading of the ER Ca2+ store could overcome the inability of IP3R receptors to release Ca2+ and suggest a luminal regulation of the receptor. To further understand how SOCE was modulating Ca2+ release we monitored lumenal ER Ca2+ levels by expressing the FRET sensor D1ER (Palmer et al., 2004). After injection of IP3, D1ER imaging revealed the depletion/reloading of the ER stores by SOCE as a function of membrane potential and time. During the long hyperpolarizing voltage jumps (SOCE) that are able to trigger a Ca2+ wave, the D1ER signal revealed that the high Ca2+ in the ER outlasts the cytoplasmic Ca2+ event leaving the IP3R facing low cytoplasmic Ca2+ concentration and high lumenal Ca2+. Together these findings shed new light on the complex regulation of the IP3R by SOCE through modulation of both cytoplasmic and lumenal Ca2+ levels.