Over 20 years ago, two groups independently domesticated Legionella pneumophila from a clinical isolate of bacteria collected during the first recognized outbreak of Legionnaires’ disease (at the 1976 American Legion’s convention in Philadelphia). These two laboratory strains, JR32 and Lp01, along with their derivatives, have been disseminated to a number of laboratories around the world and form the cornerstone of much of the research conducted on this important pathogen to date. Nevertheless, no exhaustive examination of the genetic distance between these strains and their clinical progenitor has been performed thus far. Such information is of paramount importance for making sense of several phenotypic differences observed between these strains. As environmental replication of L. pneumophila is thought to exclusively occur within natural protozoan hosts, retrospective analysis of the domestication and axenic culture of the Philadelphia-1 progenitor strain by two independent groups also provides an excellent opportunity to uncover evidence of adaptation to the laboratory environment. To reconstruct the phylogenetic relationships between the common laboratory strains of L. pneumophila Philadelphia-1 and their clinical ancestor, we performed whole-genome Illumina resequencing of the two founders of each laboratory lineage: JR32 and Lp01. As expected from earlier, targeted studies, Lp01 and JR32 contain large deletions in the lvh and tra regions, respectively. By sequencing additional strains derived from Lp01 (Lp02 and Lp03), we retraced the phylogeny of these strains relative to their reported ancestor, thereby reconstructing the evolutionary dynamics of each laboratory lineage from genomic data.