Adult Diptera burn sugar fuels at high rates in their flight motors, and most species require external sources of sugar for normal longevity. Flower nectar is usually assumed to be the main fuel source in nature. However, honeydew produced by various Homoptera is the primitive external sugar-fuel source for Diptera, and it is still a main source for many species. The pseudotracheate labellum is a “ground-plan” feature of Diptera that originated as an adaptation for obtaining sugars from honeydew. It enables flies to dissolve dry foods and then suck up the resultant fluid under cover of the labellar lobes. The labellum, thus, prevents significant water loss during feeding on dry foods. It is particularly well suited for obtaining sugars from the dried, thin films of Homoptera honeydew. The hypothesis that Diptera originally depended on honeydew explains their “dancing” behavior; their attraction to small, shiny objects; the presence of sugar receptors on their tarsi; and various basic, primitive differences between Diptera and other orders of Neoptera. These ideas are in agreement with the fossil record of Diptera and Homoptera. Homoptera were abundant in the Permian; the first undisputed Diptera appeared after the Permian in the Triassic. Flowers did not appear until much later (in the Cretaceous). The labellum gave adult Diptera access to honeydew sugars early in their evolution and enabled them to retain a more thoroughgoing aerial life.