This is the author accepted manuscript. It is currently under an indefinite embargo pending publication by eLife Sciences Publications. ; Canine transmissible venereal tumour (CTVT) is a clonally transmissible cancer that originated approximately 11,000 years ago and affects dogs worldwide. Despite the clonal origin of the CTVT nuclear genome, CTVT mitochondrial genomes (mtDNAs) have been acquired by periodic capture from transient hosts. We sequenced 449 complete mtDNAs from a global population of CTVTs, and show that mtDNA horizontal transfer has occurred at least five times, delineating five tumour clades whose distribution track two millennia of dog global migration. Negative selection has operated to prevent accumulation of deleterious mutations in captured mtDNA, and recombination has caused occasional mtDNA re-assortment. These findings implicate functional mtDNA as drivers of CTVT global metastatic spread, further highlighting the important role of mtDNA in cancer evolution. ; This work was supported by grants from the Wellcome Trust (102942/Z/13/A) and the Royal Society (RG130615), and a Philip Leverhulme Prize from the Leverhulme Trust.