Abstract Interspecific competition can drive species coexistence through niche differentiation, yet the underlying mechanisms remain unclear. Parasitoid wasps are a group of parasitic insects that rely on host nutrients to complete their development, exhibiting intense interspecific competition. Here, two parasitoid wasps, Asobara japonica and Leptopilina drosophilae are employed, which share the common host Drosophila melanogaster , as a model system to investigate the mechanisms governing species coexistence. A. japonica employs venom‐induced host manipulation to exploit older hosts is found, thereby avoiding competition and coexisting with its competitor, L. drosophilae . Through integrated multi‐omics and functional studies, a set of DUF4803‐domain venom proteins is identified that induce the apoptosis‐mediated degradation of host imaginal discs. This process elevates dilp8 expression, causing a delay in host development that is essential for the successful development of A. japonica offspring within older hosts. How gene duplication and the subsequent functional specialization of these DUF4803‐domain genes facilitated this mechanism, allowing host resource partitioning through temporal niche differentiation, is further revealed. The study suggests that this adaptive strategy minimizes evolutionary trade‐offs and advances the understanding of species coexistence mechanisms.