Junctophilin (JP)-2 tethers the plasma membrane (PM) to sarcoplasmic reticulum (SR) and enables Ca²⁺-induced Ca²⁺ release in cardiac myocytes. Previously, we have found that JP-2 is also expressed in mouse vascular smooth muscle cells (VSMCs) and facilitates functional coupling between ryanodine receptors in the SR and large-conductance Ca²⁺-activated K⁺ channels in the PM, and thus, stabilizes vascular tone. Store-operated Ca²⁺ entry (SOCE) through Ca²⁺ release-activated Ca²⁺ (CRAC) channels is known to promote the proliferation of VSMCs. The activation of CRAC channels requires PM-SR junctional sites for forming STIM1-Orai1 complexes. However, the functional coupling between JP-2 and CRAC channels in VSMCs is unknown. Among the JP family genes (JP-1, 2, 3, and 4), abundant mRNA expression of JP-2 was detected in dedifferentiated rat aortic smooth muscle cells (rASMCs). Imaging analyses using a total internal reflection fluorescent microscope revealed that JP-2 formed molecular complexes with STIM1 beneath the PM in rASMCs. The siRNA knockdown of JP-2 in rASMCs attenuated SOCE and cell proliferation. These results suggest that JP-2 promotes SOCE through CRAC channels and cell proliferation in rASMCs. JP-2 may be involved in the cell proliferation associated with vascular remodeling in arteriosclerosis.