The idea that phytopathogenic fungi associated with tree-killing bark beetles are critical for overwhelming tree defenses and incurring host tree mortality, herein called the classic paradigm (CP), has driven research on bark beetle-fungus symbiosis for decades. It has also strongly influenced our views of bark beetle ecology. We discuss fundamental flaws in the CP, including the lack of consistency of virulent fungal associates with tree-killing bark beetles, the lack of correspondence between fungal growth in the host tree and the development of symptoms associated with a successful attack, and the ubiquity of similar associations of fungi with bark beetles that do not kill trees. We suggest that, rather than playing a supporting role for the host beetle (tree killing), phytopathogenicity performs an important role for the fungi. In particular, phytopathogenicity may mediate competitive interactions among fungi and support survival and efficient resource capture in living, defensive trees.