Photosynthetic eukaryotes contain primary, secondary or tertiary plastids, depending on the source of the organelle (a cyanobacterium or a photosynthetic eukaryote). Plastid phylogeny is relatively well investigated, but molecular phylogenies have conflicted as a function of gene choice, taxon-representations, and analytical method. To better understand the influences of these variables, we performed analyses of a multi-gene data set based on 62 plastid-associated genes of 15 taxa representing the major plastid lineages. In an attempt to distinguish phylogenetic signal from non-phylogenetic patterns, we analyzed the data using a wide range of phylogenetic methods and examined the effect of covarion evolution and compositional bias. The data suggest that the chlorophyll c-containing plastids are monophyletic and acquired their plastids from the red algae after the emergence of the Cyanidiales. The relationships among chl c-containing plastids are particularly hard to resolve. This is the largest data set used for this purpose; the analyses show that cryptophyte plastids are sister to other chl c-containing plastids, and haptophyte and peridinin-containing dinoflagellate plastids are closely related.