Phylogenetic relationships, evolutionary history and systematics of tapeworms of the family Catenotaeniidae were studied using nucleotide sequences of the partial 28S nuclear rDNA (ca. 1,500 bp) and mitochondrial 12S–16S DNA (ca. 820 bp) genes. The tapeworm material consists of 29 species, including type species of the genera Catenotaenia Janicki, 1904, Catenotaenioides Haukisalmi, Hardman and Henttonen, 2010, Pseudocatenotaenia Tenora, Mas‐Coma, Murai and Feliu, 1980, Skrjabinotaenia Akhumyan, 1946, Meggittina Lynsdale, 1953, and Hemicatenotaenia Tenora, 1977. The basal phylogenetic structure of the Catenotaeniidae remains unresolved, but it is shown that most of the catenotaeniids in Eurasia and Africa comprise a large clade represented by species of Catenotaenia, Catenotaenioides, Skrjabinotaenia and Meggittina, parasitizing murid, cricetid, nesomyid and sciurid rodents. The results suggest that the divergence and early radiation of this clade have occurred in murid rodents (represented by Apodemus spp. and Mus musculus in the present material) in western Eurasia, followed by colonization of Africa, most likely independently of the colonization of their murid hosts between these continents. There is very little evidence of cophylogeny between hosts and parasites, suggesting that host transfers have played a major role in the divergence of catenotaeniids. In Africa, catenotaeniids have radiated in other murid and nesomyid rodents, and later colonized Madagascar and recolonized Eurasia. The results also show that the subfamily Skrjabinotaeniinae (including Skrjabinotaenia and Meggittina) is monophyletic, but the Catenotaeniinae (including Catenotaenia, Catenotaenioides, Pseudocatenotaenia and Hemicatenotaenia) is clearly non‐monophyletic. In addition, the genera Catenotaenia and Skrjabinotaenia were both found to be non‐monophyletic. Based on the phylogenetic and morphological evidence, several taxonomical changes, mainly new combinations, are proposed. Overall, the present results suggest that the family Catenotaeniidae is in need of major systematic revision.