Agave (Asparagaceae) is a well-known genus due to several economically and culturally important species involved in alcohol, fiber, and sugar  production. Apart from economic species, Agaves serve as ecological keystone species for many desert ecosystems and consists of over 250 species. Agave is divided into multiple subgenera based on morphology including Manfreda, Agave, and Littaea. Subgenus Manfreda consists of 52 herbaceous species that diverged early within Agave evolution. Manfreda  exhibits highly variable floral architecture compared to other Agave lineages, attracting specialist pollinators like hummingbirds and hawkmoths as well as generalist pollinator like bees. How these floral phenotypes diversified has yet to be precisely understood, as there is little molecular evidence for phylogenetic relationships of taxa within Manfreda. Here we present a robust plastome phylogeny of taxa in Manfreda across the subgenus’s distribution, integrating an extensive floral morphometric database to assess the role pollinators played in shaping the floral diversification of this group. Our phylogenetic results indicate hybridization and chloroplast capture are likely prominent in the group. Short branches of the phylogeny backbone suggest little divergence of chloroplasts during the diversification of the group. We recovered non-monophyletic origins of similar floral phenotypes, suggesting the convergent evolution of pollinator-associated syndromes. More broadly within Agave we discovered a ~1000-base pair inversion in the plastomes of non-Manfreda Agave species used in our analyses. These results directly contribute to our understanding of the origins of convergent floral phenotypes, plastome structure variation, and species diversification within Manfreda. More generally, these results will contribute to our knowledge of Agave systematics and to this system as an emerging model for studying floral evolution. Future research will incorporate nuclear genes from an Asparagaceae custom-probe set to help parse hybridization events and, hopefully, a more resolved species phylogeny for this economically and ecologically important genus.