Hematopoietic stem cell transplantation (HSCT) is followed by a period of immune-deficiency, due to a paucity in T-cell reconstitution. Underlying causes are a severely dysfunctional thymus and an impaired production of thymus-seeding progenitors in the host. Here, we addressed whether in vitro-derived human progenitor T-cells (proT) could not only represent a source of thymus-seeding progenitors but also able to influence the recovery of the thymic microenvironment. We examined whether cotransplantation of in vitro-derived human proT-cells with hematopoietic stem cells (HSCs) was able to facilitate HSC-derived T-lymphopoiesis post-transplant. A competitive transfer approach was used to define the optimal proT subset capable of reconstituting immunodeficient mice. Although the two subsets tested (proT1, CD34(+)CD7(+)CD5(-); proT2, CD34(+)CD7(+)CD5(+)) showed thymus engrafting function, proT2 cells exhibited superior engrafting capacity. Based on this, when proT2 cells were coinjected with HSCs, a significantly improved and accelerated HSC-derived T-lymphopoiesis was observed. Furthermore, we uncovered a potential mechanism by which RANKL-expressing proT2 cells induce changes in both the function and architecture of the thymus microenvironment, which favors the recruitment of bone marrow-derived lymphoid progenitors. Our findings provide further support for the use of Notch-expanded progenitors in cell-based therapies to aid in the recovery of T-cells in patients undergoing HSCT.