We integrated three distinct datasets separately focusing on mesenchymal and endothelial cells. Using a robust multi-data-set integration, we identified previously unrecognized cell types and intermediate cell states not detectable in the individual datasets. We further established specific transcriptional signatures defining subclusters and gene regulatory networks associated with putative function. Finally, scRNA-seq of human BM niche cells showed conservation between human and moused subpopulations. In conclusion, our study identifies a new layer of complexity in the taxonomy of the mouse and human BM niche and is a useful resource for understanding the role of the BM niche in the regulation of physiological and diseased human hematopoiesis.