The first sequenced mitochondrial genome of a placozoan, Trichoplax adhaerens, challenged the conventional wisdom that a compact mitochondrial genome is a common feature among all animals. Three additional placozoan mitochondrial genomes representing highly divergent clades have been sequenced to determine whether the large Trichoplax mtDNA is a shared feature among members of the phylum Placozoa or a uniquely derived condition. All three mitochondrial genomes were found to be very large, 32- to 37-kb, circular molecules, having the typical 12 respiratory chain genes, 24 tRNAs, rnS, and rnL. They share with the Trichoplax mitochondrial genome the absence of atp8, atp9, and all ribosomal protein genes, the presence of several cox1 introns, and a large open reading frame containing an intron group I LAGLIDADG endonuclease domain. The differences in mtDNA size within Placozoa are due to variation in intergenic spacer regions and the presence or absence of long open reading frames of unknown function. Phylogenetic analyses of the 12 respiratory chain genes support the monophyly of Placozoa. The similarities in composition and structure between the three mitochondrial genomes reported here and that of Trichoplax's mtDNA suggest that their uncompacted state is a shared ancestral feature to other nonmetazoans while their gene content is a derived feature shared only among the Metazoa.