Rickettsiae are well known as intracellular pathogens of animals, humans, and plants and facultative and unorganized symbionts of invertebrates. No close relative of mitochondria has yet been associated with nutritional or developmental dependency of its host cell or organism. We have found a mycetomic Rickettsia that is a strict obligatory symbiont of the parthenogenetic booklouse Liposcelis bostrychophila (Psocoptera). These rickettsiae show an evolutionary transition from a solitary to a primary mycetomic bacterium adapted to the development of its host. These intracellular and intranuclear bacteria reside in specialized cells in several tissues. Their distribution changes markedly with the development of their host. The most advanced phenotype is a paired mycetome in the abdomen, described for the first time for Rickettsia and this host order. The mycetomic rickettsiae of two parthenogenetic book lice species are in the spotted fever group and in the basal limoniae group. While mycetomic bacteria are well known for their metabolic or light-emitting functions, these rickettsiae have an essential role in the early development of the oocyte. Removal of the Rickettsia stops egg production and reproduction in the book louse. In two phylogenetically distant psocopteran species, Rickettsia are shown to be associated with four transitional stages from free bacteria, infected cells, through single mycetocytes to organ-forming mycetomes.