The cotton-melon aphid, Aphis gossypii Glover, an extremely polyphagous pest insect, comprises of sympatric populations specialized on deferent host plants. The life history of A. gossypii infesting cucurbit crops remains elusive because oviparous aphids from overwintering hosts (often hibiscus) cannot colonize cucurbit crops. We verified that the hibiscus-specialized lineage (HI) suffered high mortality and gave birth to very few nymphs developing into yellow dwarfs when transferred to fresh cucumber because the HI lineage was unable to ingest phloem sap from fresh cucumber. However, the HI lineage ingested phloem sap successfully when cucumber leaves were pre-infected with Pseudoperonospora cubensis, a biotrophic phytopathogen, accompanied by significant fitness improvement. More surprisingly, the HI lineage with feeding experience on pre-infected cucumber for two generations performed as well as the cucumber-specialized lineage (CU) did on fresh cucumber, and inflicted typical damage symptom to healthy cucumber plant. This phytopathogen mediated host plant adaptation may be widespread in polyphagous aphids.