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The peridinin pigmented dinoflagellate chloroplasts are the result of a secondary endosymbiotic event between a photosynthetic eukaryote and a dinoflagellate. Dinoflagellate chloroplast and nuclear evolution were independent before this endosymbiotic event. To reconstruct the evolution of the dinoflagellate chloroplast, phylogenies were constructed with a chloroplast gene <i>psbB</i>. The gene phylogeny should reflect the evolution of the chloroplast and indicate the plastid donor lineage. Gene sequences derived from the dinoflagellate chloroplast were extremely divergent but suggested that the plastid donor could have been a haptophyte. In an attempt to find better genes for analysis and to further understand gene transfer about 4900 randomly selected expressed genes were sequenced from two dinoflagellates, <i>Lingulodinium polyedra</i> and <i>Amphidinium carterae</i>. From these genes, thirty typically plastid-encoded genes were found, including eight otherwise known only from plastid genomes. Based on poly-A tails, gene families, and leader sequences these genes appear to be nuclear-encoded in dinoflagellates. This result suggests that dinoflagellate chloroplasts may have the smallest protein-coding potential yet known. These genes and the partially sequenced chloroplast genome of a haptophyte were used in a phylogenetic analysis. There is strong conflict between genes encoded in the chloroplast and those in the nucleus. The chloroplast genes suggest relationship between haptophyte and dinoflagellate plastids, while the nuclear-encoded genes suggest a relationship with heterokonts. Chromophyte plastid monophyly is supported by these data but the single origin of the chromophyte plastid from red algae does not mean that the host lineages are monophyletic. These results are consistent with at least two different scenarios: either dinoflagellates and haptophytes independently acquired a plastid from the heterokonts, or dinoflagellates acquired their plastids from haptophtyes, who in turn acquired their plastids from heterokonts. The evolutionary rate of the remaining plastid-encoded genes was compared with formerly plastid-encoded genes. These relative rate tests revealed strong incongruence between minicircle genes, formerly plastid-encoded genes and genes that were likely to have been acquired from the nucleus of the plastid donor lineage.