The transforming growth factor β (TGF-β) family signalling pathways are essential for normal tissue homeostasis but are often deregulated in cancer. Elucidating their role in tumour biology may inform new diagnostic and prognostic strategies. The TGF-β family pathways fall into two distinct branches, distinguished by which SMAD effector proteins are involved in the downstream signalling. TGF-β family signalling via SMAD2/3 has been extensively described and plays both tumour-suppressive and tumour-promoting roles. A similar duality has been proposed for SMAD1/5 signalling, although it is much more poorly understood. Here, I have characterised the dynamic requirement of SMAD1/5 signalling throughout tumourigenesis using an array of murine models of breast cancer. I have shown that several models of breast carcinoma exhibited no apparent activation of SMAD1/5 signalling in established growing tumours and metastases in vivo. Strikingly however, knockout of SMAD1/5 in the 4T1 and D2A1-m2 murine breast carcinoma cell lines markedly impaired orthotopic tumour growth and metastasis, suggesting that the pathway is transiently activated at discrete points during tumour development. RNA sequencing of metastatic late-stage tumour cells from the lung revealed that SMAD1/5 knockout leads to differential interaction between tumour cells and different immune cell populations compared with tumour cells wild type for SMAD1/5. More precisely, gene set enrichment analysis revealed enriched chemokine and neutrophil associated signatures in SMAD1/5 null cancer cells. These results demonstrate that SMAD1/5 signalling is dynamically regulated at different steps of tumourigenesis. Given the marked reduction in metastases upon blockade of SMAD1/5 signalling, inhibition of this pathway may represent a novel therapeutic target.