Parasitic plants have major impacts on host fitness. In the case of species of the holoparasitic Cuscuta genus, these impacts were shown to be particularly strong in some invasive alien plants, which has raised interest in the underlying mechanism. We hypothesized that Cuscuta parasitization may exert strong influence in shaping the diversity patterns in the host rhizosphere microbiome and that this may vary between native (coevolved) and alien (non-coevolved) plants. Here, we report on a field study exploring the effect of parasitization by Cuscuta australis on the rhizosphere microbiota (16S and ITS rDNA) of four plant species sharing and three plant species not sharing the parasite's native range. Despite a predominant role of the host species in shaping the rhizosphere microbiota, the role of host origin and of parasitization still appeared important in structuring microbial communities and their associated functions. Bacterial communities were more strongly influenced than fungi by the native range of the host plant, while fungi were slightly more affected than bacteria by parasitization. About 7% of bacterial phylotypes and 11% of fungal phylotypes were sensitive to Cuscuta parasitization. Parasitization also reduced the abundance of arbuscular mycorrhizal fungi by ca. 18% and of several genes related to plant growth promoting functions (e.g., nitrogen metabolism and quorum sensing). Both fungi and bacteria differentially responded to host parasitization depending on host origin, and the extent of these shifts suggests that they may have more dramatic consequences for alien than for native plants.