Stem and progenitor cells residing in the intestinal crypts drive the majority of colorectal cancers (CRCs), yet vascular contribution to this niche remains largely unexplored. Vascular endothelial growth factor A (VEGFA) is a key driver of physiological and tumor angiogenesis. Accordingly, current anti-angiogenic cancer therapies target the VEGFA pathway. Here we report that in CRC expansion of the stem/progenitor pool in intestinal crypts requires VEGFA-independent growth and remodeling of blood vessels. Epithelial transformation-induced expression of the endothelial peptide apelin, directs migration of distant venous endothelial cells toward progenitor niche vessels ensuring optimal perfusion. In the absence of apelin, loss of injury-inducible PROX1+ epithelial progenitors inhibited both incipient and advanced intestinal tumor growth. Our results establish fundamental principles for the reciprocal communication between vasculature and the intestinal progenitor niche and provide a mechanism for resistance to VEGFA-targeting drugs in CRCs.|Bernier-Latmani et al. report a mechanism for maintaining colon cancer-associated vasculature, in which colon endothelial apelin signaling promotes migration of distant venous endothelial cells toward the tumor progenitor cell niche to sustain VEGFA-independent vascular expansion and a normoxic microenvironment.