Wood-decaying Basidiomycetes are among the most efficient degraders of plant cell walls, making them key players in forest ecosystems, global carbon cycle, and in bio-based industries. Recent insights from -omics data revealed a high functional diversity of wood-decay strategies, especially among the traditional white-rot and brown-rot dichotomy. We examined the mechanistic bases of wood-decay in the conifer-specialists Armillaria ostoyae and Armillaria cepistipes using transcriptomic and proteomic approaches. Armillaria spp. (Fungi, Basidiomycota) include devastating pathogens of temperate forests and saprotrophs that decay wood. They have been discussed as white-rot species, though their response to wood deviates from typical white-rotters. While we observed an upregulation of a diverse suite of plant cell wall degrading enzymes, unlike white-rotters, they possess and express an atypical wood-decay repertoire in which pectinases and expansins are enriched, whereas lignin-decaying enzymes (LDEs) are generally downregulated. This combination of wood decay genes resembles the soft-rot of Ascomycota and appears widespread among Basidiomycota that produce a superficial white rot-like decay. These observations are consistent with ancestral soft-rot decay machinery conserved across asco- and Basidiomycota, a gain of efficient lignin-degrading ability in white-rot fungi and repeated, complete, or partial losses of LDE encoding gene repertoires in brown- and secondarily soft-rot fungi.