Ergasilidae are a family of globally distributed copepods parasitizing freshwater fish. Despite their widespread occurrence and importance for nutrient cycles, their phylogeographic patterns are poorly understood, specifically in the African Great Lakes. Here, we aim to improve the knowledge about the species diversity of copepods infecting Tylochromis polylepis, an endemic cichlid fish species in Lake Tanganyika, and about the phylogenetic relationship of African ergasilids. We present the first record of Ergasilus kandti parasitizing the gills of T. polylepis in Lake Tanganyika proper identified through light microcopy and, for the first time for any ergasilid, confocal laser scanning microscopy. Morphological analyses showed variations in numbers of spines and setae of the swimming legs. Phylogenetic analyses based on ribosomal DNA fragments suggest two monophyletic groups of African ergasilids. However, the phylogenetic relationships of Ergasilus remain unresolved because of the insufficient resolution of these widely used phylogenetic markers. A comparison of ergasilid mitochondrial genomes highlights gene order stability and interspecific length variation in rrnL. We also provide the first complete ribosomal operon of any African ergasilid and the first whole genome sequencing reads of any ergasilid. This study presents the most extensive morphological and molecular characterization of an ergasilid species to date.