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Summary: •Investigating the dispersal of the root‐pathogenic fungus Armillaria mellea is necessary to understand its population biology. Such an investigation is complicated by both its subterranean habit and the persistence of genotypes over successive host generations. As such, host colonization by resident mycelia is thought to outcompete spore infections.•We evaluated the contributions of mycelium and spores to host colonization by examining a site in which hosts pre‐date A. mellea. Golden Gate Park (San Francisco, CA, USA) was established in 1872 primarily on sand dunes that supported no resident mycelia. Genotypes were identified by microsatellite markers and somatic incompatibility pairings. Spatial autocorrelation analyses of kinship coefficients were used to infer spore dispersal distance.•The largest genotypes measured 322 and 343 m in length, and 61 of the 90 total genotypes were recovered from only one tree. The absence of multilocus linkage disequilibrium and the high proportion of unique genotypes suggest that spore dispersal is an important part of the ecology and establishment of A. mellea in this ornamental landscape.•Spatial autocorrelations indicated a significant spatial population structure consistent with limited spore dispersal. This isolation‐by‐distance pattern suggests that most spores disperse over a few meters, which is consistent with recent, direct estimates based on spore trapping data. [ABSTRACT FROM AUTHOR]