Osteocytes regulate the vascularization of transcortical vessels (TCVs) by transferring mitochondria to endothelial cells. This study shows that osteocytes maintain the normal network of TCVs by transferring mitochondria to endothelial cells in cortical bone. Partial ablation of osteocytes leads to TCV regression, while inhibition of mitochondrial transfer by conditional knockout of Rhot1 in osteocytes also causes TCV regression. Conversely, acquisition of osteocyte mitochondria by endothelial cells restores endothelial dysfunction. Administration of osteocyte mitochondria accelerates angiogenesis and healing of cortical bone defects. These findings suggest that osteocyte-TCV interactions are crucial for bone homeostasis and may inspire mitochondrial therapy for bone-related diseases. Blood vessels are essential for bone and bone marrow homeostasis, playing a critical role in bone development, wound healing, and providing a microenvironment for hematopoietic and immune cell differentiation. TCVs originate from bone marrow, traverse to cortical bone, and connect the endosteum and periosteum, facilitating communication between the inner cavity and outer shell of bone. TCVs serve as critical routes for hematopoietic cells and components, as well as bone cells and immune cell communication. Osteocytes, which make up 90–95% of all bone cells in cortical bone, are embedded in the cortical bone matrix and extend dendrites toward the mineralizing front. These dendrites form an interconnected network between osteocytes, enabling intercellular signal transmission and organelle communication. Osteocytes are the dominant cells embedded in mineralized cortical bone and play important roles in regulating bone homeostasis, suggesting they may act as critical mediators for TCV ingrowth and maintenance. The study reveals that osteocytes maintain a normal TCV network by transferring mitochondria to endothelial cells in cortical bone. The acquisition of osteocyte mitochondria maintains normal endothelial functions by alleviating oxidative stress, promoting cell proliferation, advancing tube formation, and restoring the migration capability of endothelial cells. The pro-angiogenic effect of osteocyte mitochondria on endothelial cells can be mimicked by supplementation with D-sphingosine and abolished after the inhibition of osteocytes sphingosine kinase 1 (SPHK1). These findings reveal a unique mechanism involved in the vascular homeostasis of cortical bone and potentially open up a therapeutic approach for bone diseases associated with vascular damage. The study also shows that osteocytes connect to endothelial cells of TCVs through dendrites, and their ablation leads to TCV regression. The results indicate that osteocytes regulate the vascularization of TCVs directly, independent of osteoclasts. Osteocyte-derived mitochondria are transferred to endothelial cells, which is essential for TCV vascularization. The transfer of mitochondria from osteocytes to endothelial cells is mediated by MIRO1, a critical protein of the mitochondrial transport machinery. The depletion of Rhot1Osteocytes regulate the vascularization of transcortical vessels (TCVs) by transferring mitochondria to endothelial cells. This study shows that osteocytes maintain the normal network of TCVs by transferring mitochondria to endothelial cells in cortical bone. Partial ablation of osteocytes leads to TCV regression, while inhibition of mitochondrial transfer by conditional knockout of Rhot1 in osteocytes also causes TCV regression. Conversely, acquisition of osteocyte mitochondria by endothelial cells restores endothelial dysfunction. Administration of osteocyte mitochondria accelerates angiogenesis and healing of cortical bone defects. These findings suggest that osteocyte-TCV interactions are crucial for bone homeostasis and may inspire mitochondrial therapy for bone-related diseases. Blood vessels are essential for bone and bone marrow homeostasis, playing a critical role in bone development, wound healing, and providing a microenvironment for hematopoietic and immune cell differentiation. TCVs originate from bone marrow, traverse to cortical bone, and connect the endosteum and periosteum, facilitating communication between the inner cavity and outer shell of bone. TCVs serve as critical routes for hematopoietic cells and components, as well as bone cells and immune cell communication. Osteocytes, which make up 90–95% of all bone cells in cortical bone, are embedded in the cortical bone matrix and extend dendrites toward the mineralizing front. These dendrites form an interconnected network between osteocytes, enabling intercellular signal transmission and organelle communication. Osteocytes are the dominant cells embedded in mineralized cortical bone and play important roles in regulating bone homeostasis, suggesting they may act as critical mediators for TCV ingrowth and maintenance. The study reveals that osteocytes maintain a normal TCV network by transferring mitochondria to endothelial cells in cortical bone. The acquisition of osteocyte mitochondria maintains normal endothelial functions by alleviating oxidative stress, promoting cell proliferation, advancing tube formation, and restoring the migration capability of endothelial cells. The pro-angiogenic effect of osteocyte mitochondria on endothelial cells can be mimicked by supplementation with D-sphingosine and abolished after the inhibition of osteocytes sphingosine kinase 1 (SPHK1). These findings reveal a unique mechanism involved in the vascular homeostasis of cortical bone and potentially open up a therapeutic approach for bone diseases associated with vascular damage. The study also shows that osteocytes connect to endothelial cells of TCVs through dendrites, and their ablation leads to TCV regression. The results indicate that osteocytes regulate the vascularization of TCVs directly, independent of osteoclasts. Osteocyte-derived mitochondria are transferred to endothelial cells, which is essential for TCV vascularization. The transfer of mitochondria from osteocytes to endothelial cells is mediated by MIRO1, a critical protein of the mitochondrial transport machinery. The depletion of Rhot1