Sister (congeneric) species may exhibit disparate patterns of biogeographic genetic structures due to different life histories and habitat preferences. The common cockle Cerastoderma edule and the lagoon cockle Cerastoderma glaucum probably diverged from their common ancestor in the present territory of Sahara around 5 million years ago. Although it is difficult to separate both species morphologically, various genetic markers, both mitochondrial and nuclear, clearly distinguish them. Furthermore, their lifestyles are different, as C. edule has a much less fragmented coastal habitat and a longer duration of pelagic larval stage than C. glaucum. A comparative genetic analysis was conducted on 17 populations of C. edule and 13 populations of C. glaucum using a 506 bp fragment of mitochondrial DNA (COI). We tested the hypothesis that differences in habitat types and life history are reflected in the genetic structure patterns of these two cockles. Indeed substantial differences in population genetic structures between them are revealed. Genetic diversity within C. glaucum populations decreases northwards as a consequence of post-glacial (re)colonization from southern refugia, while C. edule displays an opposite pattern indicating survival in glacial refuges in the northern Atlantic. Among populations within geographic groups, genetic differentiation is low in C. edule, probably as a result of larval dispersal with coastal currents, while it is extremely high in C. glaucum, best explained by the fragmented habitats. Interestingly, long distance divergence is less expressed in C. glaucum than in C. edule, which supports the speculation that migrating birds (frequently observed in lagoons) may occasionally transport the former more often or more efficiently than the latter. The approach applied in this study (e.g., rarefaction procedure, selection of samples of both species from the same regions) enabled a new and reliable comparative analysis of the existing raw datasets.