Phytophthora pluvialis is an oomycete that was first isolated from soil, water, and tree foliage in mixed Douglas-fir-tanoak forests of the US Pacific Northwest (PNW). It was then identified as the causal agent of red needle cast (RNC) of radiata pine (Pinus radiata) in New Zealand (NZ). Genotyping-by-sequencing (GBS) was used to obtain 1,543 single nucleotide polymorphisms (SNPs) across 145 P. pluvialis isolates to characterize the population structure in the PNW and NZ. We tested the hypothesis that P. pluvialis was introduced to NZ from the PNW using genetic distance measurements and population structure analyzes among locations between countries,. The low genetic distance, population heterozygosity, and lack of geographic structure in NZ, suggest a single colonization event from the US followed by clonal expansion in NZ. The PNW Coast Range was proposed as a presumptive center of origin of the currently known distribution of P. pluvialis based on its geographic range and position as the central cluster in a minimum spanning network. The Coastal cluster of isolates were located at the root of every US cluster, and emerged earlier than all NZ clusters. The Coastal cluster had the highest degree of heterozygosity (Hs = 0.254) and median pairwise genetic distance (0.093) relative to any other cluster. Finally, the rapid host diversification between closely related isolates of P. pluvialis in New Zealand, indicate that this pathogen has the potential to infect a broader range of hosts than is currently recognized.