The photosynthetic and basal apicomplexan Chromera velia was recently described, expanding the membership of this otherwise nonphotosynthetic group of parasite protists. Apicomplexans are alveolates with secondary plastids of red algal origin, but the evolutionary history of their nuclear genes is still actively discussed. Using deep sequencing of expressed genes, we investigated the phylogenetic affinities of a stringent filtered set of 3,151 expressed sequence tag-contigs by generating clusters with eukaryotic homologs and constructing phylogenetic trees and networks. The phylogenetic positioning of this alveolate alga was determined and sets of phyla-specific proteins extracted. Phylogenetic trees provided conflicting signals, with 444 trees grouping C. velia with the apicomplexans but 354 trees grouping C. velia with the alveolate oyster pathogen Perkinsus marinus, the latter signal being reinforced from the analysis of shared genes and overall sequence similarity. Among the 513 C. velia nuclear genes that reflect a photosynthetic ancestry and for which nuclear homologs were available both from red and green lineages, 263 indicated a red photosynthetic ancestry, whereas 250 indicated a green photosynthetic ancestry. The same 1:1 signal ratio was found among the putative 255 nuclear-encoded plastid proteins identified. This finding of red and green signals for the alveolate mirrors the result observed in the heterokont lineage and supports a common but not necessarily single origin for the plastid in heterokonts and alveolates. The inference of green endosymbiosis preceding red plastid acquisition in these lineages leads to worryingly complicated evolutionary scenarios, prompting the search for other explanations for the green phylogenetic signal and the amount of hosts involved.