Homoscleromorpha is a small group in the phylum Porifera (Sponges) characterized by several morphological features (basement membrane, acrosomes in spermatozoa, and cross-striated rootlets of the flagellar basal apparatus) shared with eumetazoan animals but not found in most other sponges. To clarify the phylogenetic position of this group, we determined and analyzed the complete mitochondrial DNA (mtDNA) sequence of the homoscleromorph sponge Oscarella carmela (Porifera, Demospongiae). O. carmela mtDNA is 20,327 bp and contains the largest complement of genes reported for animal mtDNA, including a putative gene for the C subunit of the twin-arginine translocase (tatC) that has never been found in animal mtDNA. The genes in O. carmela mtDNA are arranged in 2 clusters with opposite transcriptional orientations, a gene arrangement reminiscent of those in several cnidarian mtDNAs but unlike those reported in sponges. At the same time, phylogenetic analyses based on concatenated amino acid sequences from 12 mitochondrial (mt) protein genes strongly support the phylogenetic affinity between the Homoscleromorpha and other demosponges. Altogether, our data suggest that homoscleromorphs are demosponges that have retained ancestral features in both mt genome and morphological organization lost in other taxa and that the most recent common ancestor of sponges and other animals was morphologically and genetically more complex than previously thought.