The cilium is a characteristic organelle of eukaryotes constructed from over 600 proteins. Bacterial flagella are entirely different. 9 + 2 motile cilia evolved before the divergence of the last eukaryotic common ancestor (LECA). This chapter explores, compares, and contrasts two potential pathways of evolution: (1) via invasion of a centriolar-like virus and (2) via autogenous formation from a pre-existing microtubule-organizing center (MTOC). In either case, the intraflagellar transport (IFT) machinery that is nearly universally required for the assembly and maintenance of cilia derived from the evolving intracellular vesicular transport system. The sensory function of cilia evolved first and the ciliary axoneme evolved gradually with ciliary motility, an important selection mechanism, as one of the driving forces.