The large and diverse P450 (CYP) superfamily encodes enzymes with a wide spectrum of monooxygenase and related activities. Insect P450 enzymes of the CYP4G subfamily are known to catalyze the synthesis of cuticular hydrocarbons that serve multiple functions from desiccation resistance to chemical communication. These functions are essential for survival. In order to understand the evolution of insect CYP4G genes, 368 sequences from 24 insect orders and 167 species were mined and analyzed. The genomes of most species of Neoptera carry at least two CYP4G genes that are paralogs of the two Drosophila CYP4G genes. The duplication of the original CYP4G is basal to Neoptera and no CYP4G is found in Paleoptera, or beyond the class Insecta. The sequences of CYP4G and particularly their active site have been highly conserved over 400 MY, but all CYP4G sequences are characterized by a + 44 residue insertion between the G and H helices, which protrudes from the globular structure of the enzyme distally from the membrane anchor. Although it is generally considered that genes with highly conserved sequence and function are evolutionarily "stable", the evidence from the CYP4G subfamily shows that since their initial duplication over 400 MYA, these genes have experienced many gene births and deaths. The CYP4G1 homolog has been lost several times, and is missing in five orders of insects. These losses are both ancient, as in all Hemiptera and Thysanoptera, and more recent as in honey bees. Serial duplications leading to CYP4G gene clusters have also been observed, as in house flies and in fireflies. The detailed evolutionary history of CYP4G genes does not support the "stability" of these essential genes, but rather a "revolving door" pattern where their essential function is maintained despite an apparently random birth and death process. The dual function of cuticular hydrocarbons, in desiccation resistance achieved mainly by the quantity of hydrocarbons produced and in chemical communication, achieved by the blend of hydrocarbons produced, may explain the apparently paradoxical evolution of CYP4G genes.