The genus Ficus (Moraceae) is best known for its obligate mutualism with pollinating fig-wasps (Agaonidae), where species are thought to reciprocally trigger genetic differentiation resulting in tight co-speciation. Here, we used nextRAD DNA sequencing to study the population structure of multiple fig species and their corresponding fig-wasps along an elevational gradient in Papua New Guinea. Contrary to the expected one-to-one species specificity in this mutualism we find evidence of multiple pollinating wasp species, which through limited dispersal abilities along the gradient, likely limit pollen flow and influence fig population structure along these slopes. In two cases, where the fig species studied have wide distribution along the mountain, we found between three and four wasp species pollinating closely related populations of fig species. In the case of one fig subspecies complex, we identified two fig-wasp species according to the distribution of their host subspecies. Finally, in a parapatric, three sister species complex, we identified three individual wasp species, each corresponding to its host fig species. Fig-wasps appear to speciate more rapidly through faster generation times, faster rates of local adaptation and/or weak dispersal abilities compared to figs. This in turn restricts pollen movement between fig ecotypes, strengthening reproductive barriers and so facilitating their speciation. Fig speciation along the gradient and wasp lineage extinction may eventually restore the one-to-one rule in this mutualism through split and sort speciation dynamics.