Immune cells constitutively suppress the outgrowth of nascent malignancies in a process termed cancer immune surveillance. The vast majority of tumours arising in humans are of epithelial origin. Whereas recirculating memory CD8+ T (TCIRC) cells are largely excluded from the epithelium, tissue-resident memory T (TRM) cells reside permanently in epithelial compartments where they provide superior protection against localised infection. However, whether TRM cells also mediate tumour surveillance in peripheral tissues remains unclear. We have developed a novel murine melanoma model to elucidate the contribution of TRM cells to the regulation of peripheral tumour development. We found that epicutaneous B16 melanoma inoculation elicited expansion of naïve CD8+ T cells in skin-draining lymph nodes and subsequent accumulation of tumour-specific CD69+CD103+ skin TRM cells at the site of melanoma challenge. Presence of tumour-primed TRM cells correlated with heightened tumour control in mice failing to develop macroscopic melanoma, despite detection of dormant cancer cells in the skin of these mice long after tumour implantation. Prophylactically lodged tumour-specific TRM cells conferred protection against epicutaneous melanoma challenge in the absence of TCIRC cells. Subsequent ablation of TRM cells from mice initially protected from melanoma challenge triggered tumour outgrowth, revealing that TRM cells can suppress cancer progression by orchestrating tumour-immune equilibrium. Our work demonstrates that TRM cells form spontaneously in the tumour microenvironment, where they protect against peripheral cancer development independently of TCIRC cells by promoting a subclinical tumour equilibrium. These findings reveal a previously unrecognised role for TRM cells in tumour immune surveillance and may instruct design of improved immunotherapies.