Bone is a complex tissue populated by a highly heterogeneous mix of cell types in different compartments. The endosteal compartment is a key site for bone remodelling, a crucial process that determines and maintains bone mass. Despite the key role of the endosteal compartment in bone homeostasis and disease, the specific identity of the cells that comprise the compartment remains unclear. Our work focuses on charting the cellular and molecular landscape in bone to identify cellular mechanisms underlying the regulation of bone mineral density (BMD). Using single cell RNAseq (scRNAseq), we have identified multiple cell types in both mouse and human bones, including multiple clusters of myeloid, lymphoid, osteoblastic, chondrocytic and vascular cells, each with distinct transcriptional profiles. Integrated analysis with findings from human genetic studies of BMD identified osteoblasts, chondrocytes, and vascular cells to be enriched for BMD-associated genes. Cell type-specific BMD-associated genes were more likely to result in abnormal BMD when deleted in mice. In-depth skeletal phenotyping validated the critical functions of novel BMD-associated genes, including the endothelial cell-specific gene SLC9A3R2, which when deleted in mice resulted in reduced trabecular bone mass. Our integrative approach identifies cell types present in the endosteal compartment, including bone resident cells and vascular cells, in which genetic determinants of BMD may function to influence pathogenesis of monogenetic and polygenetic skeletal disorders with abnormal BMD. This provides a resource to prioritise genes to accelerate development of patient-centred therapeutics for skeletal diseases.