Volatile organic compound (VOC)-mediated communication between distinct fungal colonies is a crucial yet poorly understood aspect of interspecies interactions. We investigated the airborne interactions between Trichoderma atroviride (SZMC 24276) and haploid Armillaria ostoyae (SZMC 23085) hyphae using an in vitro face-off system that combined transcriptomic and gas chromatography-mass spectrometry (GC-MS) analyses. Distinct temporal VOC profiles were observed, including the early accumulation of the constitutively produced 6-pentyl-α-pyrone (6-PP) and the later appearance of 2-heptanone from T. atroviride, as well as the production of an interaction-specific cadinane-type sesquiterpene in A. ostoyae. Multi-omics integration revealed a direct coupling between transcriptional regulation and volatile output, with suppression of C8 signaling compounds such as 1-octen-3-ol and non-ribosomal peptide synthetase-associated pathways in T. atroviride under volatile exposure. In contrast, A. ostoyae exhibited extensive transcriptional reprogramming characterized by oxidative stress responses, detoxification pathways, and activation of terpene biosynthetic clusters. These findings indicate that T. atroviride constitutively produces 6-PP as a broad-spectrum volatile irritant and modulates its secondary metabolism in a context-dependent manner, while A. ostoyae responds to volatile cues through stress-associated and defensive mechanisms. Overall, this study demonstrates that VOCs function as active regulators of interactions before physical contact, shaping both metabolic and transcriptional responses, and highlights their potential role in Trichoderma-based biocontrol strategies against Armillaria.