Streptomyces species produce many important antibiotics and have a crucial role in soil nutrient cycling. However, their evolutionary history remains poorly characterized. We have evaluated the impact of homologous recombination on the evolution of Streptomyces using multi-locus sequence analysis of 234 strains that represent at least 11 species clusters. Evidence of inter-species recombination is widespread but not uniform within the genus and levels of mosaicism vary between species clusters. Most phylogenetically incongruent loci are monophyletic at the scale of species clusters and their subclades, suggesting that these recombination events occurred in shared ancestral lineages. Further investigation of two mosaic species clusters suggests that genes acquired by inter-species recombination may have become fixed in these lineages during periods of demographic expansion; implicating a role for phylogeography in determining contemporary patterns of genetic diversity. Only by examining the phylogeny at the scale of the genus is apparent that widespread phylogenetically incongruent loci in Streptomyces are derived from a far smaller number of ancestral inter-species recombination events.