New Guinea is the largest tropical island in the world and hosts immense endemic biodiversity. However, our understanding of how the gradual emergence of the terrestrial ecosystems of the island over the last 40 Myr has generated this biological richness is hampered by poorly documented species diversity and distributions. Here, we address both these issues through an integrative taxonomy and biogeographical approach using Hylophorbus, a New Guinea-endemic genus of frogs with 12 recognized species. We delimited candidate species by integrating mitochondrial DNA, nuclear DNA, and bioacoustics, then investigated their evolutionary history. Our results suggest that the current taxonomy of the genus misses true species diversity by ≥3.5-fold. Nevertheless, most candidate species (27) remain unconfirmed because of missing data, whereas five were identified unambiguously as undescribed (we describe three of these formally). Time-calibrated phylogenetic analyses suggest that Hylophorbus diversification began ~9 Mya in the northern or eastern portion of New Guinea. It would appear that lineages dispersed to new terrestrial habitats in the west, notably uplifted by the central range orogeny, until eventually reaching the Bird’s Head during the Mio-Pliocene (7–5 Mya). Conversely, a past barrier appears to have prevented north–south dispersal. These data suggest that new habitat availability has primarily driven the diversification of Hylophorbus.