Emerging technologies have paved the way for exploring the balance between stochasticity and determinism in regulating stem cell fate. Recent advances have enabled the ex-vivo expansion of murine HSPCs, while preserving their inherent ability to reconstitute the haematopoietic system in mice. However, as ex-vivo expansion of HSPCs results in functional and transcriptional heterogeneity, the relationship between the transcriptional program and subsequent cell fate outcome in-vivo remains poorly understood. Here, we coupled an optimised method to expand murine HSPCs ex-vivo with a modified version of our expressed barcoding technology, SPLINTR (single-cell profiling and lineage tracing)-V3. Barcoded HSPCs isolated from murine bone marrow were expanded for defined time periods of up to five weeks prior to transplantation into several mice. In these experiments, we preserved a portion of the culture just prior to transplantation and transplanted an identical population of HSPCs clones into several mice. This strategy enabled us to assess how the cell-intrinsic chromatin landscape and transcriptional properties of ex-vivo expanded HSPCs influences output and cell fate decisions in-vivo. Our findings suggest that despite extensive ex-vivo propagation, clonal engraftment and contribution to different haematopoietic lineages is remarkably preserved in sister-clones across different mice. We observed that the cell-intrinsic properties of HSPCs not only regulated the overall clonal output, but also determined the proportion of clonal contribution to different lineages in recipient mice. Moreover, the clones that exhibited multilineage fate outcomes had the highest lineage output in the recipient mice. Using single-cell RNAseq analysis on cells prior to transplantation, we observed a diversity in clonal behaviour, resulting in the transcriptional heterogeneity observed in the culture. Additionally, among the engrafted clones, the in-vitro clonal behaviour mirrored the in-vivo fate outcome. Overall, our study provides new insights into how ex-vivo expansion of HSPCs influences output and cell fate in-vivo.