Genetic studies of Lessepsian species often demonstrate the absence of a genetic bottleneck in a wide plethora of taxa, from plants to fish, but information regarding the genetic responses of their parasites in the newly colonized ecosystems is still lacking. This study compared genetic diversity of Red Sea (Eilat, Nabq), Suez canal (Ismailia) and Mediterranean (Rhodes, Tel Aviv) populations of the Monogenoidea Glyphidohaptor plectocirra by sequencing a portion of the mitochondrial CoxI gene. Despite evidence of a slight decrease in the genetic diversity of Mediterranean populations, a simulation analysis based on coalescent theory demonstrated the absence of significant bottlenecks, but there was directional selection along a cline moving further from the Suez canal. The absence of bottlenecks was congruent with that described for G. plectocirra hosts Siganus rivulatus and Siganus luridus, and reflected a common history of high propagule pressure during initial colonization, and constant or repeated gene flow from the Red Sea to the Mediterranean area. However, directional selection was peculiar to the parasites and likely originated from parasite genotype 9 environment interactions. Finally, an anisotropic contribution of Red Sea populations to the Lessepsian invasion was demonstrated.