Allopolyploid hybridization instantly merges two differentially adapted genomes into one individual. Allopolyploids are often evolutionarily successful, undergoing adaptive radiations despite the genetic and physiological challenges of merging genomes. We examine a suite of induced herbivore resistance traits in three independent lines of the synthetic allopolyploid Nicotianaxmierata (Nma) and its parent species, N. miersii (Nmi) and N. attenuata (Na), to determine how a complex polygenetic adaptation fares during the early stages of neoallopolyploid formation. All species responded to Manduca sexta oral secretions (OS) with a temporally prolonged jasmonate (JA) burst. In one parent (Na), the JA burst was additionally amplified and associated with the elicitation of direct and indirect defenses. In the other parent (Nmi), OS neither amplified the JA burst nor elicited defense responses, although applied MeJA confirmed the inducibility of the defense responses. All lines of Nma retained enough aspects of Na's JA signaling to recognize OS and to accumulate sufficient direct defenses to impair the growth of Manduca larvae. Most defense-related metabolites were retained in Nma even if inherited from only one parent; however, OS-elicited volatiles, trypsin protease inhibitors (TPIs) and chlorogenic acid were lost in some lines, even though MeJA treatment elicited similar responses in all lines. Herbivore defense systems are flexibly inherited in allopolyploids, causing individuals to diverge over only a few generations; for example, line 1 of Nma could not produce TPIs after OS elicitation, whereas lines 2 and 3 could. This flexible integration of defense signaling systems with a diversity of elicited responses may explain why adaptive radiations are commonly found in allopolyploid lineages.