Transcortical vessels (TCVs) play a crucial role in facilitating communication between the bone marrow vascular system and the external circulation. Osteocytes, the primary cells in cortical bone, are found to maintain the normal network of TCVs by transferring mitochondria to the endothelial cells lining the TCVs. Partial ablation of osteocytes leads to TCV regression, and inhibiting mitochondrial transfer by conditional knockout of *Rho1* in osteocytes also results in TCV network regression. Conversely, the acquisition of osteocyte mitochondria by endothelial cells effectively restores endothelial dysfunction, including alleviating oxidative stress, promoting cell proliferation, advancing tube formation, and enhancing migration. Administration of osteocyte mitochondria accelerates angiogenesis and bone defect healing. These findings provide new insights into the interaction between osteocytes and TCVs and suggest potential therapeutic applications for mitochondrial therapy in bone-related diseases.Transcortical vessels (TCVs) play a crucial role in facilitating communication between the bone marrow vascular system and the external circulation. Osteocytes, the primary cells in cortical bone, are found to maintain the normal network of TCVs by transferring mitochondria to the endothelial cells lining the TCVs. Partial ablation of osteocytes leads to TCV regression, and inhibiting mitochondrial transfer by conditional knockout of *Rho1* in osteocytes also results in TCV network regression. Conversely, the acquisition of osteocyte mitochondria by endothelial cells effectively restores endothelial dysfunction, including alleviating oxidative stress, promoting cell proliferation, advancing tube formation, and enhancing migration. Administration of osteocyte mitochondria accelerates angiogenesis and bone defect healing. These findings provide new insights into the interaction between osteocytes and TCVs and suggest potential therapeutic applications for mitochondrial therapy in bone-related diseases.