Cilia and flagella play a crucial role in the development and function of eukaryotes. The activity of thousands of dyneins is precisely regulated to generate flagellar motility. The complex proteome (600+ proteins) and architecture of the structural core of flagella, the axoneme, have made it challenging to dissect the functions of the different complexes, like the regulatory machinery. Previous reports suggested that the flagellum of American eel sperm lacks many of the canonical axonemal complexes yet is still motile. Here, we use cryo-electron tomography for molecular characterization of this proposed "minimal" motile flagellum. We observed different diameters for the eel sperm flagellum: narrow at the base and wider towards the flagellar tip. Subtomogram averaging revealed the 3D-structure of the eel sperm flagellum. As expected, major complexes were missing, e.g., outer dynein arms, radial spokes, and the central-pair-complex, but we found molecular remnants of most complexes. We also identified bend-direction specific patterns in the inter-DMT distance in actively beating eel sperm flagella and we propose a model for the regulation of dynein activity during their motility. Together, our results shed light on the structure and function of the eel sperm flagellum and provide insight into the minimum requirements for ciliary beating. [Media: see text].