Island archipelagos are well known for promoting geographic and adaptive radiations in terrestrial animals. Sympatry of closely related species in island systems has been thought to occur primarily through double-invasions from the same continental source population. Alternatively, this process can occur on a smaller geographic scale where divergent populations isolated from one another within an archipelago may come back into contact via intra-archipelago dispersal. Depending on degree of divergence and the development of reproductive isolating barriers, the result of this secondary contact could be gene flow between isolated populations, exclusion or extirpation of one population via competition, or the establishment of reproductively isolated sympatric species. Here, we provide strong evidence for intra-archipelago secondary sympatry within a radiation of Phylloscopus warblers in the Solomon and Bismarck archipelagos by presenting the first well-sampled phylogeny of Phylloscopus warbler populations in the region. By using genome-wide genetic data and complete mitochondrial genomes we also present evidence for a complex history of mitochondrial-nuclear discordance within this radiation, particularly in the only pair of sympatric populations east of Wallace’s Line, located on Kolombangara Island in the Solomon Islands. Our genomic data suggest that the divergent single-island endemic species on Kolombangara (Phylloscopus amoenus) is not a relic resulting from a double invasion from outside the Bismarck and Solomon archipelagos as previously thought. Rather, the sympatry on Kolombangara Island between the widespread P. poliocephalus and the endemic P. amoenus appears to result from recent intra-archipelago diversification, either via sympatric speciation or the rapid establishment of secondary sympatry. These novel genomic data provide insights into the evolutionary history of Phylloscopus warblers in Melanesia and improve our general understanding of how biodiversity accumulates in island systems.