Intramembranous and endochondral ossifications are two essential process of bone formation. It has been shown that the terminally differentiated osteocytes in intramembranous and endochondral ossifications are derived from mesenchymal cells and chondrocyte respectively. However, little is known if osteocytes derived from these two different ancestors have different geometrical and metabolic properties. In this study, we employed confocal structured illumination microscopy (SIM) and mRNA-seq analysis to characterize the geometrical properties of osteocytes from calvaria formed by intramembranous ossification and cortical bone formed by endochondral ossification. SIM and geometrical mathematical modelling revealed that calvarial osteocytes are round shaped with radiated dendritic processes, while cortical osteocytes are spindle shaped with perpendicular dendrites. Calvarial osteocytes are more randomly arranged within the bone matrix, while cortical osteocytes are orderly arranged with paralleled distributions of dendritic network along the axis of cortical bone. Further, mRNA-seq analysis detected 8445 genes were differentially expressed, in which 121 genes were ossification-related. We also observed upregulation of Inppl1, Mapk3, Mtss1, Nf1, Plxnb1, Ptk2b, Smad3, Tacr1 and Bmp5 and downregulation of Alox15, Id1, Tac1, Ranbp3l in cortical osteocytes as compared to that in calvarial osteocytes. The varied expression of these cytoskeleton organization and dendrite development related genes may regulate the morphological differences of osteocytic cell bodies and dendrites. Finally, we showed that aging mainly affects the cortical osteocytes but not calvarial osteocytes. Aging causes distortion of osteocyte dendrites, and the deflection of osteocyte cell bodies in cortical bone but not calvarial bone. Together, in this study we suggest that there are two types of osteocytes, depending on the process of ossification.