Radiotherapy, a treatment modality received by more than half of all cancer patients, remains one of the most effective approaches to achieve local tumour control. Despite technological advances, healthy tissue injury due to off-target radiation exposure can still occur. In our study, we exposed healthy mouse lung tissue to radiation prior to the induction of metastasis, to understand the biological link between tissue damage and cancer progression. Radiation-induced lung injury resulted in a strong enhancement of metastatic colonization, driven by enhanced regenerative Notch signalling. Importantly, locally activated neutrophils were found to be key drivers of these tissue perturbations, profoundly increasing the metastatic proficiency of irradiated lung tissue and endowing arriving cancer cells with an augmented stemness phenotype. These findings not only reveal a novel tumour-supportive function of neutrophils in the context of tissue-injury, but also have important clinical implications by suggesting targeting their activity could enhance the success of radiotherapy for the treatment of cancer.