Thelohanellus Kudo, 1933 is a species rich genus of Myxosporea, sharing many morphological similarities with species of Myxobolus but the former possesses a single polar capsule, and the latter has two. Based on molecular phylogenetic analyses, this single distinguishing feature is not monophyletic, and members of Thelohanellus are intermixed with Myxobolus species, calling into question the validity of genus Thelohanellus. The occurrence of two polar capsules in a small proportion of Thelohanellus spores as observed in this study suggests that these species have the capacity to express this Myxobolus-like trait, clouding the distinction of these two genera further. Herein, using the most comprehensive data set to date, we explored the phylogenetic relationships of Thelohanellus to other myxobolids, to investigate the evolutionary history of the genus Thelohanellus and the origins of single polar capsule in this group. The phylogenetic analyses and statistical tests of topology revealed Thelohanellus as a strongly supported polyphyletic lineage, clustering in five distinct branches within Myxobolus clade. Ancestral state reconstruction for polar capsule number showed that Thelohanellus species have evolved from myxosporean species with two polar capsules at least four times, which could be classified in three possible evolutionary pathways. The polyphyly of Thelohanellus and the multiple evolutionary origins of single polar capsule of Thelohanellus demonstrate that the distinction of this genus from Myxobolus is largely for convenience, and does not reflect their evolutionary history.