Emerging pathogens have been increasing exponentially over the last century. The knowledge on whether these organisms are native to ecosystems or have been recently introduced is often of great importance. Understanding the ecological and evolutionary processes promoting emergence can help to control their spread and forecast epidemics. Using restriction site-associated DNA sequencing data, we studied genetic relationships, pathways of spread, and evolutionary history of Phellinus noxius, an emerging root-rotting fungus of unknown origin, in eastern Asia, Australia, and the Pacific Islands. We analyzed patterns of genetic variation using Bayesian inference, maximum likelihood phylogeny, populations splits and mixtures measuring correlations in allele frequencies and genetic drift, and finally applied coalescent based theory using approximate Bayesian computation (ABC) with supervised machine learning. Population structure analyses revealed five genetic groups with signatures of complex recent and ancient migration histories. The most probable scenario of ancient pathogen spread is movement from west to east: from Malaysia to the Pacific Islands, with subsequent spread to Taiwan and Australia. Furthermore, ABC analyses indicate that P. noxius spread occurred thousands of generations ago, contradicting previous assumptions that it was recently introduced in multiple areas. Our results suggest that recent emergence of P. noxius in east Asia, Australia, and the Pacific Islands is likely driven by anthropogenic and natural disturbances, including deforestation, land-use change, severe weather events, and introduction of exotic plants. This study provides a novel example of utilization of genome wide allele frequency data to unravel dynamics of pathogen emergence under conditions of changing ecosystems.