Athymic cytokine receptor γ chain mutant mice that lack the thymus, Peyer's patches, cryptopatches (CP), and intestinal T cells were reconstituted with wild-type bone marrow cells. Bone marrow–derived TCR⁻ intraepithelial lymphocytes (IEL) first appeared within villous epithelia of small intestine overlying the regenerated CP, and these TCR⁻ IEL subsequently emerged throughout the epithelia. Thereafter, TCR⁺ IEL increased to a comparable number to that in athymic mice and consisted of TCRγδ and TCRαβ IEL. In gut-associated lymphoid tissues of wild-type mice, only CP harbored a large population of c-kit^highIL-7R⁺CD44⁺Thy-1^+/−CD4^+/−CD25^low/−α_Eβ₇⁻Lin⁻ (Lin, lineage markers) lymphocytes that included cells expressing germline but not rearranged TCRγ and TCRβ gene transcripts. These findings provide direct evidence that gut CP develop progenitor T cells for extrathymic IEL descendants.