We present the first, most comprehensive, phylogenetic hypothesis for holodonates based on a combination of molecular (12S rDNA, 16S rDNA, 18S rDNA, 28S rDNA, COII, and Histone 3) and morphological (153 characters) data for the majority of extant and fossil lineages (255 taxa). To address questions concerning the evolution of flight within the group, the combined data was analyzed under a parsimony framework. Hypotheses concerning the evolution of flight within the group have long been controversial, namely the number of origins for petiolate wings. When only extant taxa are considered there is no clear picture of flight evolution. Only by including a large diversity of fossil lineages does a clear picture of flight evolution emerge. Results indicate holodonates began as gliders, transitioned to hoverers and today posses an amazingly agile flight. Further, the development of wing characteristics, such as the arculus and nodus, serve to strengthen and stiffen the wing during flight and appear to be correlated throughout holodonate evolutionary history.