Recombination in the control region (CR) of Mytilus mitochondrial DNA (mtDNA) was originally reported based on the relatively short, sequenced fragments of mitochondrial genomes. Recombination outside the CR has been reported recently with the suggestion that such processes are common in Mytilus. We have fully sequenced a set of 11 different mitochondrial haplotypes representing the high diversity of paternally inherited mitochondrial genomes of Baltic Sea Mytilus mussels, including the haplotype close to the native Mytilus trossulus mitochondrial genome, which was thought to have been entirely eliminated from this population. Phylogenetic and comparative analysis showed that the recombination is limited to the vicinity of the CR in all sequenced genomes. Coding sequence comparison indicated that all paternally inherited genomes showed increased accumulation of nonsynonymous substitutions, including the genomes which switched their transmission route very recently. The acquisition of certain CR sequences through recombination with highly divergent paternally inherited genomes seems to precede and favor the switch, but it is not a prerequisite for this process. Interspecies hybridization in the Baltic Sea during the recent 10,000 years created conditions for both structural and evolutionary mitochondrial instability which resulted in the observed variation and dynamics of mtDNA in Baltic Sea Mytilus mussels. In conclusion, the data shows that the effects of mitochondrial recombination are limited to the CR of few phylogenetic lineages.