CD4+ and CD8+ conventional T cells (Tconv) differentiate from double-positive thymocytes into naive T cells in the human thymus under the regulation of known transcriptional programs driven by ThPOK and RUNX3. However, very little is known about the development of human iNKT, MAIT and γδT cells, collectively known as innate T cells (Tinn). Our current knowledge is limited to studies in mouse models where distinct gene regulatory programs induce the direct differentiation of Tinn thymocytes into effector T cells, contrasting with Tconv development. We thus compared cell states and regulatory transcriptional programs driving Tconv and Tinn development following their positive selection in human pediatric thymi, to evaluate the translational relevance of mouse studies to human thymopoiesis. To that end we leveraged fluorescence-activated cell sorting strategies and single-cell transcriptomics, which revealed a large fraction of human iNKT and MAIT thymocytes resembling Tconv thymocytes, and only a small fraction exhibiting an effector gene signature. Through cross-species comparisons, we found some human iNKT and MAIT thymocytes in a "naive-like" state mimicking CD4+ and CD8+ Tconv naive states respectively, that is absent from their murine counterpart. The few effector Tinn thymocytes in human do not subdivide into the three previously defined murine effector subtypes, but rather into one (for MAIT and γδT cells) or two (for iNKT cells) subtypes. Furthermore, we found evidence suggesting that human Tinn thymocytes likely migrate to the thymic medulla during their differentiation, further indicating more commonalities between Tinn and Tconv developments in humans compared to mice. Contrasting Tconv and Tinn development in mice and humans has not only the potential to inform translational implications of mouse studies, but also to uncover gene regulatory programs driving human Tinn cell fate into functional effector T cells.