<p>Hybridization in plants with specialized pollination systems provides insights into the mechanisms of species boundary maintenance and breakdown. The significance of hybridization in the history of ecologically important fig trees is unclear. <i>Ficus hispida</i> and <i>Ficus squamosa</i> are dioecious species with contrasting habitats and dispersal mechanisms. We combined phenological, morphological and genomic analyses to characterize putative hybrids and interspecific gene flow. Overlapping fruiting periods during Thailand’s rainy season potentially allow reciprocal movement of pollinators between the two species. Putative hybrid individuals displayed intermediate morphological traits but had larger leaves. Genomic analyses using single nucleotide polymorphisms confirmed the hybrid status of individuals identified by their morphology. They also revealed patterns of genetic admixture with parent species. Phylogenetic analysis of chloroplast genomes also suggested historical introgression events between the two species. The hybrids were generally found in riparian areas habitats required by <i>F. squamosa</i>, where environmental conditions may be intermediate with the drier open conditions favored by <i>F. hispida</i>. Fig tree pollination depends on fig wasps that are generally host-species specific, but clearly some host switching occurs. <i>Ficus squamosa</i> has highly modified seeds adapted for dispersal by water, whereas <i>F. hispida</i> depends on seed dispersal by vertebrates. Aquatic-dispersal modifications are poorly developed in the hybrids, suggesting they require seed dispersal by frugivores. This study provides evidence of hybridization between two fig tree species with contrasting ecological preferences, but the evolutionary consequences of the inter-specific pollen-flow remain uncertain.</p>