PDGFRA-expressing mesenchymal cells provide a crucial niche for the self-renewing intestinal epithelium. Corresponding compartments remain unclear in the stomach, where corpus and antral glandular epithelia have similar niche dependencies but are structurally distinct from the intestine and from each other. Previous studies considered antrum and corpus as a whole and did not assess niche functions. We applied high-resolution approaches to identify regional subpopulations and niche properties of purified corpus and antral PDGFRA (+) cells. PDGFRA (Hi) sub-epithelial myofibroblasts are the principal sources of BMP ligands in both gastric segments, fall into two molecularly distinct groups that distribute asymmetrically along antral glands, and fail to support epithelial organoids in vitro . In contrast, PDGFRA (Lo) cells expressing CD55 from either segment uniquely enable corpus and antral organoid growth in the absence of other cellular or soluble factors. Our study provides detailed insights into spatial and functional organization of gastric mesenchyme and the spectrum of signaling sources.