The genus Carpobrotus N.E.Br. comprises between 12 and 25 species, most of which are native to South Africa. Some Carpobrotus species are considered among the most damaging invasive species in coastal dune systems worldwide. In their introduced areas, these species represent a serious threat to native species and significantly impact soil conditions and geochemical processes. Despite being well studied, the taxonomy of Carpobrotus remains problematic, as the genus comprises a complex of species that hybridize easily and are difficult to distinguish from each other. To explore the population genetic structure of invasive Carpobrotus species (i.e., C. acinaciformis and C. edulis) across a significant part of their native and non-native ranges, we sampled 40 populations across Argentina, Italy, New Zealand, Portugal, South Africa, Spain, and the USA. We developed taxon-specific microsatellite markers using a Next Generation Sequencing approach to analyze the population genetic structure and incidence of hybridization in native and non-native regions. We identified three genetically distinct clusters, which are present in both the native and non-native regions. Based on a set of selected morphological characteristics, we found no clear features to identify taxa morphologically. Our results suggest that the most probable sources of global introductions of Carpobrotus species are the Western Cape region of South Africa and the coastline of California. We suggest that management actions targeting Carpobrotus invasions globally should focus on preventing additional introductions from the east coast of South Africa, and on searching for prospective biocontrol agents in the Western Cape region of South Africa.