Scots pine (Pinus sylvestris L.) is a key species in boreal forests, valued both economically and ecologically, in part due to its associations with foliar fungi. These fungi influence plant health, nutrient cycling, and resistance induction. To investigate these interactions, we collected 1367 needle and shoot samples across 12 plus tree genotypes grown in 4 progeny trials in Estonia. Amplifying the ITS1-5.8S-ITS2 gene region, we obtained over 1.3 million high-quality sequences and identified 1261 fungal OTUs at the 98% species hypothesis level. Among the identified OTUs, 24.6% were classified as saprotrophic and 18.2% as pathogenic fungi. Fungal diversity varied significantly between tree tissue types, progeny trial locations, and plus tree origins. Fungal community composition varied across tissue types, with older needles tending to harbor more complex communities. Plus trees 593 and 267-1 progenies stood out for their high phyllosphere fungal richness, and genotype-specific correlations indicated associations between fungal diversity and tree height or needle retention, suggesting potential genotype-dependent effects on tree performance. Heritability of fungal diversity between ramets in seed orchard and progeny trees was found for saprotrophic fungi but was negligible for total fungi and pathogens, indicating strong influence of microclimate conditions. These findings underscore the potential value of integrating fungal community traits into Scots pine breeding programs. Considering microbial associations alongside traditional growth traits may help identify genotypes better suited for future forestry needs under changing environmental conditions. Additionally, Setomelanomma holmii is reported here as a new fungal pathogen on Scots pine shoots in Estonia.