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Whole‐genome surveys of genetic diversity and geographic variation often yield unexpected discoveries of novel structural variation, which long‐read DNA sequencing can help clarify. Here, we report on whole‐genome phylogeography of a bird exhibiting classic vicariant geographies across Australia and New Guinea, the blue‐faced honeyeater (Entomyzon cyanotis), and the discovery and characterization of a novel neo‐Z chromosome by long‐read sequencing. Using short‐read genome‐wide SNPs, we inferred population divergence events within E. cyanotis across the Carpentarian and other biogeographic barriers during the Pleistocene (~0.3–1.7 Ma). Evidence for introgression between nonsister populations supports a hypothesis of reticulate evolution around a triad of dynamic barriers around Pleistocene Lake Carpentaria between Australia and New Guinea. During this phylogeographic survey, we discovered a large (134 Mbp) neo‐Z chromosome and we explored its diversity, divergence and introgression landscape. We show that, as in some sylvioid passerine birds, a fusion occurred between chromosome 5 and the Z chromosome to form a neo‐Z chromosome; and in E. cyanotis, the ancestral pseudoautosomal region (PAR) appears nonrecombinant between Z and W, along with most of the fused chromosome 5. The added recombination‐suppressed portion of the neo‐Z (~37.2 Mbp) displays reduced diversity and faster population genetic differentiation compared with the ancestral‐Z. Yet, the new PAR (~17.4 Mbp) shows elevated diversity and reduced differentiation compared to autosomes, potentially resulting from introgression. In our case, long‐read sequencing helped clarify the genomic landscape of population divergence on autosomes and sex chromosomes in a species where prior knowledge of genome structure was still incomplete.