In mammals, the primitive streak region and its descendant, the tail bud, are the source of nascent mesoderm and spinal cord throughout axial elongation. A localised population of long-term axial progenitors has been identified in a region of the tail bud, the chordoneural hinge, but the localisation of such progenitors at earlier stages is so far untested. By studying gene expression, we have shown that a specific topological arrangement of domains persists from the streak to the tail bud, and includes an area (the node-streak border) in which ectoderm that expresses primitive streak markers overlies the prospective notochord. This arrangement persists in the chordoneural hinge. Homotopic grafts show that, as in other vertebrates, cells in the streak and node predominantly produce mesoderm, whereas those in the node-streak border and lateral to the streak additionally produce neurectoderm. Node-streak border descendants populate not only neurectoderm, somites and notochord throughout the axis, but also the chordoneural hinge. Ectoderm lateral to the embryonic day (E)8.5 streak is later recruited to the midline, where it produces somites and chordoneural hinge cells, the position of which overlaps that of border-derived cells. Therefore, the E8.5 axial progenitors that will make the tail comprise cells from two distinct sources: the border and lateral ectoderm. Furthermore, heterotopic grafts of cells from outside the border to this region also populate the chordoneural hinge. Expression of several streak- and tail bud-specific genes declines well before elongation ends, even though this late population can be successfully transplanted into earlier embryos. Therefore, at least some aspects of progenitor status are conferred by the environment and are not an intrinsic property of the cells.