The 3D folding of the genome is tightly linked to its epigenetic state which maintains gene expression programmes. Although the relationship between gene expression and genome organisation is highly context dependent, 3D genome organisation is emerging as a novel epigenetic layer to reinforce and stabilise transcriptional states. Whether regulatory information carried in genome folding could be transmitted through mitosis is an area of active investigation. In this review, we discuss the relationship between epigenetic state and nuclear organisation, as well as the interplay between transcriptional regulation and epigenetic genome folding. We also consider the architectural remodelling of nuclei as cells enter and exit mitosis, and evaluate the potential of the 3D genome to contribute to cellular memory.