Bone marrow is a common metastatic site for multiple solid tumours and is associated with poor prognosis and significant morbidity. Accumulating evidence indicates that cancer cells colonise specialised niches within the bone marrow to facilitate long-term propagation, but the precise location and mechanisms that support niche interactions are unknown. Using breast cancer as a model of solid tumour metastasis to the bone marrow, we applied large scale quantitative three-dimensional imaging to characterise temporal changes in the bone marrow microenvironment during metastasis formation. We show that mouse mammary tumour cells preferentially home to a pre-existing domain enriched for type H vessels. During expansion of metastases, tumour cells remodel the local vasculature through extensive sprouting to establish a supportive microenvironment. This process appears to be largely driven by tumour-derived granulocyte-colony stimulating factor (G-CSF), which stimulates endothelium through direct and indirect mechanisms. Pharmacological inhibition of G-CSF receptor normalizes intratumoural vascular remodelling and enhances survival. These findings elucidate a new mechanism of ‘host’ hijack by which mammary tumour cells subvert the local microvasculature to form a specialised, protumorigenic niche.