Halophila stipulacea, a small seagrass species native to the Indo-Pacific, is a Lessepsian migrant and a high-profile invader that has successfully colonized two exotic regions, the Mediterranean (first observed in 1894) and the Caribbean (2002). In 1961, an intracellular phytomyxid parasite, Marinomyxa marina (SAR: Rhizaria: Endomyxa: Phytomyxea) was discovered in the petioles of H. stipulacea in the Red Sea, and three decades later, it was reported off the coast of Sicily (Mediterranean), suggesting parallel migration of the two organisms. In 2018, infected petioles of H. stipulacea were also observed in St. Eustatius (Caribbean), but the identity of the causative agent remained unresolved. Here, we provide information on four new localities of phytomyxid-infested populations of H. stipulacea in Greece (Mediterranean), and Bonaire and Martinique (Caribbean), including notes on infection prevalence and seasonal dynamics. Using the 18S rRNA barcoding gene, we bring molecular evidence that the disease is caused by a genetically uniform variant of M. marina at all the examined sites. We conclude that the parasite is now widespread throughout both invaded regions and has been present in the Caribbean since 2013 at the latest. For the first time, the production of fruits in infected plants is observed, indicating a non-lethal nature of the symbiosis. While the arrival of M. marina to the Caribbean is unlikely to alleviate the current invasiveness of H. stipulacea, we emphasize the need for its further monitoring since the host-specificity and general biology of seagrass-associated phytomyxids are still poorly understood.