A heterodimer of the insect chemoreceptors Gr21a and Gr63a has been shown to be the carbon dioxide receptor in Drosophila melanogaster (Meigen) (Diptera: Drosophilidae). Comparison of the genes encoding these two proteins across the 12 available drosophilid fly genomes allows refined definition of their N-termini. These genes are highly conserved, along with a paralog of Gr21a, in the Anopheles gambiae, Aedes aegypti, and Culex pipiens mosquitoes, as well as in the silk moth Bombyx mori and the red flour beetle Tribolium castaneum. In the latter four species we name these three proteins Gr1, Gr2, and Gr3. Intron evolution within this distinctive three gene lineage is considerable, with at least 13 inferred gains and 39 losses. Surprisingly, this entire ancient gene lineage is absent from all other available more basal insect and related arthropod genomes, specifically the honey bee, parasitoid wasp, human louse, pea aphid, waterflea, and blacklegged tick genomes. At least two of these species can detect carbon dioxide, suggesting that they evolved other means to do so.