The tick-borne Rickettsiale Ehrlichia ruminantium (E. ruminantium) is the causative agent of heartwater in Africa and the Caribbean. Heartwater, responsible for major losses on livestock in Africa represents also a threat for the American mainland. Three complete genomes corresponding to two different groups of differing phenotypes, Gardel and Welgevonden, have been recently described. One genome (Erga) represents the Gardel group from Guadeloupe Island and two genomes (Erwo and Erwe) belong to the Welgevonden group. Erwo, isolated in South Africa, is the parental strain of Erwe, which was maintained for 18 years in Guadeloupe under different culture conditions than Erwo. The three strains display genomes of differing sizes with 1,499,920 bp, 1,512,977 bp, and 1,516,355 bp for Erga, Erwe, and Erwo, respectively. Gene sequences and order are highly conserved between the three strains, although several gene truncations could be pinpointed, most of them occurring within three regions of accumulated differences (RAD). E. ruminantium displays a strong leading/lagging compositional bias inducing a strand-specific codon usage. Finally, a striking feature of E. ruminantium is the presence of long intergenic regions containing tandem repeats. These repeats are at the origin of an active process, specific to E. ruminantium, of genome expansion/contraction based on the addition or removal of tandem units.