Stimulation of T-cell receptors (TCRs) through formation of the immunological synapse (IS) between antigen-presenting cells and T-cells is a necessary step for the generation of the adaptive immune response. Engagement of TCRs triggers several signalling cascades including a rise in the cytosolic Ca2+ concentration ([Ca2+ ]i) through the activation of CRAC/ORAI channels. Here we show that the CRAC/ORAI-mediated Ca2+ influx was completely dependent on the translocation of mitochondria not only towards the plasma membrane (PM) but also to the IS in an actin cytoskeleton manner, which in turn prevented Ca2+ dependent inactivation of the channels. By using epifluorescence, 2-photon and total internal reflection microscopy, we observed that a large fraction of mitochondria moved into the immediate vicinity of IS. However, maximal store depletion without formation of the IS by TCR stimulation with antibodies or pharmacological disruption of actin cytoskeleton prevented mitochondrial translocation and subsequent [Ca2+ ]i rises. The increased [Ca2+ ]i signals following formation of the IS correlated also with an enhanced T-cell proliferation. Our data, therefore, show that the distance between a PM bound signalling complex (the IS) and an organelle (mitochondria) is important to control cellular signals.