The plastids of chlorarachniophytes were derived from an ancestral green alga via secondary endosymbiosis. Thus, genes from the “green” lineage via secondary endosymbiotic gene transfer (EGT) are expected in the nuclear genomes of the Chlorarachniophyta. However, several recent studies have revealed the presence of “red” genes in their nuclear genomes. To elucidate the origin of such “red” genes in chlorarachniophyte nuclear genomes, we carried out exhaustive single-gene phylogenetic analyses, including two operational taxonomic units (OTUs) that represent two divergent sister lineages of the Chlorarachniophyta, Amorphochlora amoeboformis ( = Lotharella amoeboformis; based on RNA sequences newly determined here) and Bigelowiella natans (based on the published genome sequence). We identified 10 genes of cyanobacterial origin, phylogenetic analysis of which showed the chlorarachniophytes to branch with the red lineage (red algae and/or red algal secondary or tertiary plastid-containing eukaryotes). Of the 10 genes, 7 demonstrated robust monophyly of the two chlorarachniophyte OTUs. Thus, the common ancestor of the extant chlorarachniophytes likely experienced multiple horizontal gene transfers from the red lineage. Because 4 of the 10 genes are obviously photosynthesis- and/or plastid-related, and almost all of the eukaryotic OTUs in the 10 trees possess plastids, such red genes most likely originated directly from photosynthetic eukaryotes. This situation could be explained by a possible cryptic endosymbiosis of a red algal plastid before the secondary endosymbiosis of the green algal plastid, or a long-term feeding on a single (or multiple closely related) red algal plastid-containing eukaryote(s) after the green secondary endosymbiosis.