Fruit doves of the genus Ptilinopus (Columbidae) form a large group of more than 50 species that have been successful in colonizing most of the Pacific Ocean, with sympatric species on several small oceanic islands. A recent new phylogeny of this genus and allies by Cibois and coworkers showed that all these cases of sympatry derived from multiple independent colonizations, with the exception of the Marquesas Islands (eastern Polynesia), where the two fruit doves that occurred sympatrically are sister species: the Red-moustached Fruit Dove, Ptilinopus mercierii, and the White-capped Fruit Dove, Ptilinopus dupetithouarsii. Both Marquesas fruit doves coexisted on several Marquesas islands until the recent extinction of the Red-moustached Fruit Dove. Here, we analyze their morphology, review their life history, and discuss the two most likely scenarios for the divergence of the two species, in light of the geological history of the Marquesas hot-spot volcanoes (5.5–1.1 Ma). The microallopatry scenario takes into account the large initial size of the islands and involves partitioning of the fruit doves' distributions within the same island, whereas in the intra-archipelago scenario, the birds' speciation occurred on different islands, in conjunction with their sequential emergence. We discuss both hypotheses and conclude that estimated time of divergence of the two species and known ecology of the birds favor the intra-archipelago scenario.