Abstract Arbuscular mycorrhizal fungi may promote growth and stress resilience of plants, particularly under water-deficit conditions. However, interactions among mycorrhizal fungi, wheat plants, and aphids like the English grain aphid Sitobion avenae (Hemiptera: Aphididae) under water-deficit stress are still not well understood. Here, we examined the colonization of the fungus Claroideoglomus etunicatum (Glomerales: Claroideoglomeraceae) on wheat, and its effects on development and behavior of S. avenae under different water regimes. The symbiosis between C. etunicatum and wheat tended to increase the total developmental times of S. avenae nymphs under water deficit, but decreased adult lifespans. Irrespective of water conditions or wheat cultivars (Xinong-979 and Chang-6794), this symbiosis tended to cause higher adult weights and fecundities of S. avenae. These findings suggested that inoculation of this fungus could induce some life history trait trade-offs for S. avenae. Inoculation of C. etunicatum caused significant increases in contents of total amino acids in Xinong-979, and contents of some individual amino acids (e.g., glutamine) in both cultivars. This aphid preferred settling on symbiotic plants, with alate individuals attracted to well-watered Xinong-979 from 4 and Chang-6794 from 24 h postrelease. Increased phloem feeding and reduced pathway phase time for S. avenae were found in symbiotic plants. The fungus C. etunicatum also significantly enhanced wheat growth, especially under water deficit, and increased contents of nonessential and essential amino acids in Xinong-979. Our results highlight complex interactions among fungus symbiosis, wheat cultivars, and water conditions, emphasizing the potential to boost wheat crop resilience in the context of global climate change.