Pseudotsuga menziesii var. menziesii (coast Douglas-fir) is a tree of ecological, economic, and cultural value in its native North American Pacific Northwest (PNW) distribution. P. menziesii is host to a variety of well-documented endophytic foliar microorganisms, including the fungus Nothophaeocryptopus gaeumannii, the causal agent of Swiss needle cast (SNC), and the oomycete Phytophthora pluvialis, which causes cryptic disease symptoms in P. menziesii. Little is understood about how entire foliar microbial communities are structured by geography, climate, and host lineage, nor how foliar fungi and oomycetes interact at the tree level. This study used a large-scale reciprocal transplant experiment, next-generation sequencing (NGS), and culture-based methods to characterize the diversity and structure of foliar fungi and oomycetes of P. menziesii across three sites on the PNW coast. Fungal community composition within trees was structured by host location (p = 1e-4, 1.5e-3) as well as interactions between host location and lineage (p = 0.02, 6.4e-3, 8e-4). Oomycete communities were dominated by a single OTU, assigned to Phytophthora cacuminis, a recently described species in Australia. An undescribed Pythium species was isolated in culture from 18 trees throughout the study sites. Generalized linear mixed models revealed that fungal community richness was positively correlated to oomycete community richness among trees (estimated coefficient = 0.14, p = 8.3e-16), and that presence of P. cacuminis negatively predicted presence of N. gaeumannii (estimated coefficient = -0.65, p = 0.03). This raises questions about P. cacuminis’ presence and origins in the PNW as well as its effects on tree health. This study is among the first to use NGS to describe P. menziesii’s foliar fungal community and to characterize nonpathogenic oomycetes residing in P. menziesii needle tissue. It illustrates the need for further experimental research to identify biotic drivers of microbial community assembly, as well as the downstream implications for forest management.