The genus Asparagus comprises approximately 200 species, some of which are commercially cultivated, such as the garden asparagus (A. officinalis). Many Asparagus species, including A. officinalis, are dioecious and have been grouped into a subgenus distinct from that of hermaphroditic species. Although many interspecific crossings have been attempted to introduce useful traits into A. officinalis, only some of the dioecious species were found to be cross-compatible with A. officinalis. Here, molecular phylogenetic analyses were conducted to determine whether interspecific crossability is proportional to the genetic distance between the crossing pairs and to further clarify the evolutionary history of the Asparagus genus. A clade with all cross-compatible species and no cross-incompatible species was recovered in the phylogenetic tree based on analyses of non-coding cpDNA regions. In addition, a sex-linked marker developed for A. officinalis amplified a male-specific region in all cross-compatible species. The phylogenetic analyses also provided some insights about the evolutionary history of Asparagus; for example, by indicating that the genus had its origin in southern Africa, subsequently spreading throughout the old world through intensive speciation and dispersal. The results also suggest that dioecious species were derived from a single evolutionary transition from hermaphroditism in Asparagus. These findings not only contribute towards the understanding of the evolutionary history of the genus but may also facilitate future interspecific hybridization programs involving Asparagus species.