Telocytes are large mesenchymal cells expressing the transcription factor FOXL1, recently shown to support intestinal epithelium, by providing the essential Wnt proteins required for stem cell function. In order to create a topological map of single telocytes along the crypt-villus axis, we performed telocyte single cell RNAseq analysis combined with antibody staining and/or single molecule RNA FISH (smFISH) for landmark genes. We have identified a subpopulation of telocytes labeled by the cell-adhesion protein Spondin1 (F-Spondin) and the protein kinase Doublecortine like Kinase 1 (DCLK1) which is localized both in humans and mice along the mid crypt region where proliferating epithelial cells reside. Screening for mouse colorectal cancer model such as APCmin and human colorectal cancer tissue revealed high distribution of this subpopulation surrounding proliferating tumor cells, suggesting a role in colorectal cancer progression.