The Mariana islands of the Western Pacific are the largest and the most populous in all Micronesia. At the southern end of the Mariana archipelago is the island and U.S. territory of Guam. Guam is among the first islands ever settled as well as the first Spanish colony in Remote Oceania. The people of Guam, the CHarmoru, are also among the most diverse in the region, most likely a factor of colonial and wartime history, rather than Guam’s prehistory, which studies have shown was one of cultural and genetic isolation. In this study we analyzed the genomic markers from 65 self-identified CHamoru: Over 130,000 bi-parentally in-herited autosomal DNA markers, and approximately 7,500 and 3,200 uni-parentally inherited Y chromosome and mitochondrial DNAs (mtDNA) markers, respectively. We compared modern DNA and ancient genomes from Guam to those from the Philippines, Wallacea, Papua New Guinea, and other Pacific regions, in order to assess CHamoru origins, and identify the consequences of war and colonization on island diversity. The maternally-inherited mtDNA shows connections to the eastern regions of Wallacea as well as West Papua, with estimated time of divergence from those populations 3,000 to 4,000 years ago. The Y chromosome DNA, however, shows affinity to parts of the Philippines, as well as Wallacea, patterns indicative of both early prehistoric settlement, as well as historic migration of Filipino men to Guam during and after Spanish colonization. The autosomal DNA, in contrast, shows a much wider diversity, inclusive of ancestry from Europe, also seen in the Y DNA, as well as indigenous American, likely resulting from Mexican migrants to Guam during the Manila Galleon trade that lasted hundreds of years. The differing results from multiple genomic markers suggest that to understand the history of a population, a comprehensive look across differently-inherited DNAs is necessary.