Studying monozygotic twins who present with identical cancers informs on the developmental origins of childhood tumours. Here, we perform whole genome sequencing on multiple tumour, normal, and placental samples to reconstruct the phylogeny of a soft tissue cancer that spread in utero between monozygotic twins. We demonstrate the origin of the tumour from one twin and time its diversification and transplacental spread to the other twin, showing that the spread occurred only once. This generalisable and scalable approach additionally allows us to dissect the earliest stages of twinning, revealing unexpected asymmetrical contributions of embryonic lineages to the placenta and each twin and challenging the classical model of twinning.