The evolutionary history and relationship between plastids of dinoflagellate algae and apicomplexan parasites have been controversial both because the organelles are unusual and because their genomes contain few comparable genes. However, most plastid proteins are encoded in the host nucleus and targeted to the organelle, and several of these genes have proved to have interesting and informative evolutionary histories. We have used expressed sequence tag (EST) sequencing to generate gene sequence data from the nuclear genome of the dinoflagellate Heterocapsa triquetra and inferred phylogenies for the complete set of identified plastid-targeted proteins. Overall, dinoflagellate plastid proteins are most consistently related to homologues from the red algal plastid lineage (not green) and, in many of the most robust cases, they branch with other chromalveolate algae. In resolved phylogenies where apicomplexan data are available, dinoflagellates and apicomplexans are related. We also identified two cases of apparent lateral, or horizontal, gene transfer, one from the green plastid lineage and one from a bacterial lineage unrelated to plastids or cyanobacteria.