Haematopoietic stem cell transplantation (HSCT) provides a potentially curative strategy for >100,000 paediatric and adult cancer patients worldwide each year. However, infection-related morbidity/mortality remains a major impediment, particularly until T-cell immunity is restored. Thus, there is an urgent need to discover novel approaches to accelerate T-cell production after HSPC transplantation (HSCT). Using SPLINTR-SR, an advanced lineage tracing system with expressed barcodes, we precisely delineate at single clone resolution the cell-intrinsic and microenvironmental influences on rapid HSPC engraftment and T-cell reconstitution post HSCT. Through a clone-splitting strategy, we establish that engraftment potential, lineage commitment and clonal output are cell-intrinsic properties of HSPCs. Surprisingly, pre-existing cytopenia in the host does not redirect inherent HSPC lineage commitment programs upon HSCT but instead increases the output of specific HSPC clones to cater for the lineage-deficient need. A systematic dissection of bone marrow homing and thymic seeding after HSCT revealed a rare subset of HSPC clones that have cell-intrinsic properties for rapid and high-output T-cell reconstitution. Underpinning this potential is a novel HSPC transcription program including prominent expression of an uncharacterised gene Xlr4b. Through exogenous expression of Xlr4b in HSPCs, we demonstrate a bone marrow lymphoid differentiation trajectory that preferences T-lineage reconstitution. Clonally resolved analysis thus outlines a future path to rapidly generate T-cells for a wide range of therapeutic applications.