We sequenced and annotated the complete mitochondrial (mt) genomes of four closely related Rhynchosporium species that diverged ∼14,000–35,000 years ago. During this time frame, three of the mt genomes expanded significantly due to an invasion of introns into three genes (cox1, cox2, and nad5). The enlarged mt genomes contained ∼40% introns compared to 8.1% in uninvaded relatives. Many intron gains were accompanied by co-conversion of flanking exonic regions. The comparative analysis revealed a highly variable set of non-intronic, free-standing ORFs of unknown function (uORFs). This is consistent with a rapidly evolving accessory compartment in the mt genome of these closely related species. Only one free-standing uORF was shared among all mt genomes analyzed. This uORF had a mutation rate similar to the core mt protein-encoding genes, suggesting conservation of function among the species. The nucleotide composition of the core protein-encoding genes significantly differed from those of introns and uORFs. The mt mutation rate was 77 times higher than the nuclear mutation rate, indicating that the phylogeny inferred from mt genes may better resolve the phylogenetic relationships among closely related Rhynchosporium species than phylogenies inferred from nuclear genes.