Heterokont members of the Pelagophyceae form the massive brown tides that have continually plagued the coastal regions of the eastern U.S. seaboard and the Gulf of Mexico. To gain a better understanding of the photosynthetic competence that may be linked to their success in forming massive blooms, we sequenced the chloroplast genomes of two pelagophytes: Aureococcus anophagefferens Hargraves et Sieburth and Aureoumbra lagunensis D. A. Stockw., DeYoe, Hargraves et P. W. Johnson. The chloroplast genomes of A. anophagefferens (89,599 bp) and Ar. lagunensis (94,346 bp) are significantly smaller than those of six other stramenopiles sequenced to date. The structure (or configuration) is partially due to the absence of the large inverted repeats common in chloroplast genomes. Eight of 10 small and tandem repeats from the A. anophagefferens and Ar. lagunensis genomes are adjacent to genes coding for photosynthetic or energy production functions, implying that these domains may have functional constraints. High genomic synteny, a multigene phylogenetic analysis, and a synapomorphic change in the form of an attenuated psbA gene confirm that A. anophagefferens and Ar. lagunensis are closely related taxa. Finally, the presence of three light-independent chl-biosynthesis genes in the chloroplast of Ar. lagunensis, but absence in the chloroplast and nuclear genomes of A. anophagefferens, suggests the persistence of a more ancient (i.e., dark-adaptive) potential in Ar. lagunensis but not in A. anophagefferens. Whether the presence of both chl-biosynthesis pathways in Ar. lagunensis contributes to the ability of this organism to sustain prolonged bloom (continuously for ∼8 years) under reduced light conditions, but not A. anophagefferens (a few months), remains an open question.