Breast cancer is the most common cancer in women worldwide. Despite improved screening and treatment in the early stages of tumor development, it remains difficult to treat stages of cancer when metastatic processes are underway. Metastatic development is based in particular on the acquisition by cancer cells of migration capacities, involving remodeling of the cytoskeleton, which is highly dependent on the intracellular calcium ion concentration. While research has focused on the involvement of membrane ion channels in migration processes, the role of the Orai3 calcium channel in migration processes remains unknown. By cationic imaging and live-cell imaging, we showed that the Orai3 channel constitutively allows the entry of calcium essential in the migration of two breast cancer lines: MDA-MB-231 and MDA-MB-231 BrM2 (n = 3; Student t-test and ANOVA test; p < 0.001). We found that Orai3 silencing decreased cell migration along with a decrease in the basal calcium entry into these lines. Furthermore, the pharmacological activation of Orai3 with 2-Amino-Ethyl Borate (2-APB) leads to an increase in cell migration. Moreover, we demonstrated the impact of Orai3 expression in breast cancer cell lines morphology through the modulation of the cytoskeleton. Indeed, Orai3 knockdown greatly decreased the polymerization of F-actin filaments, and cells lacking Orai3 expression presented a rounded cell morphology and failed to exhibit stress fibers compared to cells expressing Orai3 (n = 3; ANOVA test; p < 0.001). Finally, we investigated the mechanisms of cell adhesion through the study of the activity of calpain. Our results showed that Orai3, through its ability to modulate calcium entry allows for the activation of calpain, which is required to modulate cell adhesion and migration processes.  This indicates that Orai3 drives intracellular calcium dynamics necessary for migration processes and for cytoskeleton remodeling of breast cancer cells (n = 3; ANOVA test; p < 0.001). Interestingly, we also noticed the adhesion forces to the extracellular matrix, which were determined by single-cell force spectroscopy, were not altered in any way (N = 3; Student t-test), suggesting a regulation of adhesion and migration processes through a signaling pathway underlying Orai3. In conclusion, our results reveal a key role of Orai3 in breast cancer cell migration by regulating actin cytoskeleton remodeling and cell adhesion correlated with the modulation of basal calcium entry.