The ability to reprogram cell morphogenesis in response to environmental cues is fundamental to microbial adaptation and survival. The nematode-trapping fungus Arthrobotrys oligospora exemplifies this plasticity by developing adhesive traps to capture nematodes. This morphological transition involves spatial reorientation of cell polarity, cytoskeletal remodeling, and cell fusion. However, the molecular mechanisms that coordinate these processes remain unclear. Using live-cell imaging, genetics, and functional assays, we demonstrated that cell polarity proteins localize to hyphal tips to direct growth, while actin and septins assemble at the curving inner rim to shape trap architecture. Conserved NADPH oxidases are induced by the presence of nematodes and are required for the recruitment of cell polarity proteins and cytoskeletal factors to promote trap cell fusion. Together, these findings reveal that polarity cues, cytoskeletal organization, and reactive oxygen species signaling are integrated to orchestrate nematode-induced trap development, establishing nematode-trapping fungi as a versatile model to study fungal cell biology.