Intercellular mitochondrial transfer has attracted a great deal of attention for its major role in the regulation of tissue damage, tissue homeostasis, inflammation and resistance to cancer chemotherapy. Osteocytes are an excellent model to investigate the mechanism of mitochondrial transfer, since osteocytes form an inter-connecting network through their dendritic processes. We demonstrated, in primary murine osteocytes with photo-activatable mitochondria (PhAM)floxed and in MLO-Y4 cells, mitochondrial transfer in the dendritic networks, visualized by high resolution confocal imaging. Normal, healthy osteocytes transferred mitochondria to adjacent metabolically stressed osteocytes depleted of functional mitochondria and restored their metabolic function. Remarkably, the coordinated movement and transfer of mitochondria within the dendritic network rely on endoplasmic reticulum (ER)-mitochondria contact, predominantly mediated by mitofusin 2 (Mfn2), a GTPase that tethers ER to mitochondria. A decline in Mfn2 expression with age occurs concomitantly with impaired mitochondrial distribution and transfer in the osteocyte dendritic network. These data show a previously unknown function of ER-mitochondrial contact in mediating mitochondrial transfer, and provides a mechanism to explain the complex homeostasis of osteocytes.