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To better understand functional ecology of bark beetle-microbial symbioses, we characterized yeast associates of North American spruce beetle (Dendroctous rufipennis Kirby) across populations. Seven yeast species were detected; Wickerhamomyces canadensis (Wickerham) Kurtzman et al. (Sachharomycetales: Saccharomycetaceae) was the most common (74% of isolates) and found in all populations. Isolates of W. canadensis were subsequently tested for competitive interactions with symbiotic (Leptographium abietinum, = Grosmannia abietina) and pathogenic (Beauvaria bassiana) filamentous fungi, and isolates were nutritionally profiled (protein and P content). Exposure to yeast headspace emissions had isolate-dependent effects on colony growth of symbiotic and pathogenic fungi; most isolates of W. canadensis slightly inhibited growth rates of symbiotic (L. abietinum, mean effect: − 4%) and entomopathogenic (B. bassiana, mean effect: − 6%) fungi. However, overall variation was high (range: − 35.4 to + 88.6%) and some yeasts enhanced growth of filamentous fungi whereas others were consistently inhibitory. The volatile 2-phenylethanol was produced by W. canadensis and synthetic 2-phenylethanol reduced growth rates of both L. abietinum and B. bassiana by 36% on average. Mean protein and P content of Wickerhamomyces canadensis cultures were 0.8% and 7.2%, respectively, but isolates varied in nutritional content and protein content was similar to that of host tree phloem. We conclude that W. canadensis is a primary yeast symbiont of D. rufipennis in the Rocky Mountains and emits volatiles that can affect growth of associated microbes. Wickerhamomyces canadensis isolates vary substantially in limiting nutrients (protein and P), but concentrations are less than reported for the symbiotic filamentous fungus L. abietinum.