Motility generated by 9+2 organelles, variably called cilia or flagella, evolved before divergence from the last common ancestor of extant eukaryotes. In order to understand better how motility in these organelles is regulated, evolutionary steps that led to the present 9+2 morphology are considered. In addition, recent advances in our knowledge of flagellar assembly, together with heightened appreciation of the widespread role of cilia in sensory processes, suggest that these organelles may have served multiple roles in early eukaryotic cells. In addition to their function as undulating motility organelles, we speculate that protocilia were the primary determinants of cell polarity and directed motility in early eukaryotes, and that they provided the first defined membrane domain for localization of receptors that allowed cells to respond tactically to environmental cues. Initially, motility associated with these protocilia may have been gliding motility rather than the more complex bend propagation. Once these protocilia became functional motile organelles for beating, we believe that addition of an asymmetric central apparatus, capable of transducing signals to dynein motors and altering beat parameters, provided refined directional control in response to tactic signals. This paper presents hypothesized steps in this evolutionary process, and examples to support these hypotheses.