As humans and mice age, the composition of their immune compartment changes, with a depletion of lymphoid cells and an expansion of myeloid cells. Ageing hematopoietic stem cells (HSCs) show changes in gene expression and chromatin accessibility that somewhat associate with this myeloid bias and there is good evidence that systemic chronic inflammation contributes to this stem cell phenotype. However, efforts to reverse the myeloid bias by modulating inflammatory signalling have only been partially successful. We explored if there is also some cell-intrinsic ageing process that contributes to immune cell dysfunction. We used in situ Hi-C to map the interactions between chromatin regions of old and young murine HSCs, and compared this to gene expression, chromatin accessibility and histone mark data, to build a picture of the gene regulatory network. The differences in the chromatin interactions between old and young HSCs indicate that myeloid pathways are indeed activated, but there is also a detectable increase in informational entropy and changes leading to lineage-inappropriate gene expression. Our work further demonstrates that age-related epigenetic changes likely contribute to HSC aging and functional decline.