Throughout much of the range of western white pine, Pinus monticola Dougl., timber harvesting, fire exclusion and the presence of Cronartium ribicola J. C. Fisch., the white pine blister rust (WPBR) pathogen, have led to negative population and genetic consequences. To address these interactions, we examined population dynamics and genetic diversity in 10 populations of western white pine in upper montane forests of the Lake Tahoe Basin. We documented negative population trends for three of the 10 populations. These populations exhibited low estimated growth rates (λ), moderate to high incidences of WPBR and mountain pine beetle (MPB), and high levels of mortality. In contrast, seven populations appear to be stable (λ ≥ 1.0), with low to moderate disease and insect incidence, and evidence for genetic resistance to WPBR. Genetic diversity (HE) for a set of 160 single nucleotide polymorphisms was in the range of 0.245–0.272 across populations, and population-specific estimates of FST ranged from 0.0062 to 0.0244. Allele frequency of the Cr2 gene, which confers complete resistance to C. ribicola in western white pine, was low, averaging 0.009 for all populations sampled. However, a low frequency of pollen receptors (i.e., susceptible maternal parents pollinated by a local resistant parent) was found in nine of 10 populations. A moderate and negative relationship was found between the frequency of pollen receptors in a population and the incidence of WPBR (r2 = 0.32). In the context of an introduced pathogen, climate driven outbreaks of MPB, fire exclusion, and prolonged drought, conservation and management strategies are warranted for this species in the Lake Tahoe Basin and likely other locations in California. These strategies include gene conservation of western white pine, WPBR resistance screening, and forest restoration treatments.