Aphis gossypii and Helicoverpa armigera are two important agricultural pests in cotton plants. However, whether early colonization of A. gossypii affects subsequent H. armigera is unknown. We implemented ecological experiments to reveal that A. gossypii-damaged cotton plants [Bacillus thuringiensis (Bt) and non-Bt] had a significant avoidance effect on the oviposition preference of H. armigera adults. However, A. gossypii-damaged cotton plants (non-Bt) increased the weight and pupation rate and reduced the mortality of H. armigera larvae. Transcriptomic and metabolomic analyses showed that 13 and 9 genes were significantly upregulated to be involved in salicylic acid (SA) and indole acetic acid (IAA) biosynthesis, and SA and IAA contents were significantly increased, respectively. However, 15 genes involved in jasmonic acid (JA) biosynthesis were significantly downregulated as a result of the antagonism of SA and JA. Moreover, there was significant upregulation in multiple genes involved in the biosynthesis of L-histidine, fructose, maltotetraose, melezitose, lecithin, stearidonic acid, and mannitol, in which metabolites were confirmed to promote the growth and development of H. armigera. Our study is a reference for investigating the evolutionary relationships and provides insights into implementing effective insect biocontrol between H. armigera and A. gossypii.