Some volatile compounds (VC) play critical roles in intra- and interspecies interactions. To investigate roles of VC in fungal ecology, we characterized how VC produced by Verticillium spp., a group of broad-host-range soilborne fungal pathogens, affect plant growth and development. VC produced by 19 strains corresponding to 10 species significantly enhanced the growth of Arabidopsis thaliana and Nicotiana benthamiana. Analysis of VC produced by four species revealed the presence of diverse compounds, including those previously shown to affect plant growth. Using A. thaliana, we investigated the mechanism underpinning plant growth enhancement by Verticillium dahliae VC. Allometric analysis indicated that VC caused preferential resource allocation for root growth over shoot growth. Growth responses of A. thaliana mutants defective in auxin or ethylene signaling suggested the involvement of several components of auxin signaling, with TIR3 playing a key role. AUX1, TIR1, and AXR1 were also implicated but appeared to play lesser roles. Inhibition of auxin efflux using 1-naphthylphthalamic acid blocked VC-mediated growth enhancement. Spatial and temporal expression patterns of the auxin-responsive reporter DR5::GUS indicated that the activation of auxin signaling occurred before enhanced plant growth became visible. Results from this study suggest critical yet overlooked roles of VC in Verticillium ecology and pathology.