Abstract Transposable elements (TEs) are an important factor shaping eukaryotic genomes. Although a significant body of research has been conducted on the abundance of TEs in nuclear genomes, TEs in mitochondrial genomes remain elusive. In this study, we successfully assembled 28 complete yeast mitochondrial genomes and took advantage of the power of population genomics to determine mobile DNAs and their propensity. We have observed compelling evidence of GC clusters propagating within the mitochondrial genome and being horizontally transferred between species. These mitochondrial TEs experience rapid diversification by nucleotide substitution and, more importantly, undergo dynamic merger and shuffling to form new TEs. Given the hyper mobile and transformable nature of mitochondrial TEs, our findings open the door to a deeper understanding of eukaryotic mitochondrial genome evolution and the origin of nonautonomous TEs.