Enzymes performing the initial reaction of aromatic amino acid biosynthesis, 2-keto-3-deoxy-D-arabino-heptulosonate 7-phosphate (DAHP) synthases, exist as two distinct homology classes. The three classic Escherichia coli paralogs are AroA_I proteins, but many members of the Bacteria possess the AroA_II class of enzyme, sometimes in combination with AroA_I proteins. AroA_II DAHP synthases until now have been shown to be specifically dedicated to secondary metabolism (e.g., formation of ansamycin antibiotics or phenazine pigment). In contrast, here we show that the Xanthomonas campestris AroA_II protein functions as the sole DAHP synthase supporting aromatic amino acid biosynthesis. X. campestris AroA_II was cloned in E. coli by functional complementation, and genes corresponding to two possible translation starts were expressed. We developed a 1-day partial purification method (>99%) for the unstable protein. The recombinant AroA_II protein was found to be subject to an allosteric pattern of sequential feedback inhibition in which chorismate is the prime allosteric effector. L-Tryptophan was found to be a minor feedback inhibitor. An N-terminal region of 111 amino acids may be located in the periplasm since a probable inner membrane-spanning region is predicted. Unlike chloroplast-localized AroA_II of higher plants, X. campestris AroA_II was not hysteretically activated by dithiols. Compared to plant AroA_II proteins, differences in divalent metal activation were also observed. Phylogenetic tree analysis shows that AroA_II originated within the Bacteria domain, and it seems probable that higher-plant plastids acquired AroA_II from a gram-negative bacterium via endosymbiosis. The X. campestris AroA_II protein is suggested to exemplify a case of analog displacement whereby an ancestral aroA_I species was discarded, with the aroA_II replacement providing an alternative pattern of allosteric control. Three subgroups of AroA_II proteins can be recognized: a large, central group containing the plant enzymes and that from X. campestris, one defined by a three-residue deletion near the conserved KPRS motif, and one possessing a larger deletion further downstream.