In the thymus, 2 types of Lin^–Sca-1⁺ (lineage-negative stem cell antigen-1–positive) progenitors can generate T-lineage cells: c-Kit^hi interleukin-7 receptor α–negative (c-Kit^hiIL-7Rα^–) and c-Kit^loIL-7Rα⁺. While c-Kit^hiIL-7Rα^– progenitors are absent, c-Kit^loIL-7Rα⁺ progenitors are abundant in the lymph nodes (LNs). c-Kit^loIL-7Rα⁺ progenitors undergo abortive T-cell commitment in the LNs and become arrested in the G₁ phase of the cell cycle because they fail both to up-regulate c-myb, c-myc, and cyclin D2 and to repress junB, p16^INK4a, and p21^Cip1/WAF. As a result, development of LN c-Kit^loIL-7Rα⁺ progenitors is blocked at an intermediate CD44⁺CD25^lo development stage in vivo, and LN-derived progenitors fail to generate mature T cells when cultured with OP9-DL1 stromal cells. LN stroma can provide key signals for T-cell development including IL-7, Kit ligand, and Delta-like–1 but lacks Wnt4 and Wnt7b transcripts. LN c-Kit^loIL-7Rα⁺ progenitors are able to generate mature T cells when cultured with stromal cells producing wingless-related MMTV integration site 4 (Wnt4) or upon in vivo exposure to oncostatin M whose signaling pathway intersects with Wnt. Thus, supplying Wnt signals to c-Kit^loIL-7Rα⁺ progenitors may be sufficient to transform the LN into a primary T-lymphoid organ. These data provide unique insights into the essence of a primary T-lymphoid organ and into how a cryptic extrathymic T-cell development pathway can be amplified.