The important role of flagellates in aquatic microbial food webs is mediated by their flagella that enable them to swim and generate a feeding current. The flagellum in most predatory flagellates is equipped with rigid hairs that reverse the direction of thrust compared to the thrust due to a smooth flagellum. Conventionally, such reversal has been attributed to drag anisotropy of individual hairs, neglecting their hydrodynamic interactions. Here, we show that hydrodynamic interactions are key to thrust-generation and reversal in hairy flagellates, making their hydrodynamics fundamentally different from the slender-body theory governing microswimmers with smooth flagella. Using computational fluid dynamics and model analysis, we demonstrate that long and not too closely spaced hairs and strongly curved flagellar waveforms are optimal for thrust-generation. Our results form a theoretical basis for understanding the diverse flagellar architectures and feeding modes found in predatory flagellates.