Abstract Cover crops are multifunctional tools that mitigate environmental impacts of agriculture, enhance resilience to weather extremes and suppress weeds and arthropod pests. Cover crops provide non‐crop food and habitat resources that attract natural enemies of pests, but their outcomes for pest management are less clear in regions where keystone mutualisms between red imported fire ants and aphids dominate. Here, we manipulate ant exclusion treatments and cover crop treatments (living mulches and terminated cover crops) that vary in food/habitat resources and examine responses of ants, aphids, other herbivores and predators in a cotton agroecosystem. Living mulches reduced both ants and aphids in the crop canopy by 97% and 93%, respectively, relative to bare soil treatments, and terminated cover crops reduced them as well by a lesser degree (~50%). Non‐aphid herbivores occurred in low densities system‐wide and increased in living mulches, whilst native predators had variable responses to cover crops and ant exclusion. Cover crops had no effect on prey removal in the crop canopy, but living mulches tripled rates of weed seed biocontrol, relative to bare soils. Cover crops elicited a shift in fire ant foraging from cotton foliage downward to the soil‐surface, preventing competitive exclusion by keystone ant/aphid mutualists that dominate crop monocultures. Cover crops altered the system‐wide impacts of fire ants: reducing ecosystem disservices (i.e. aphid tending) and enhancing ecosystem services (i.e. weed seed biocontrol). These results provide incentives for cover crop adoption as a regenerative practice in large‐scale commercial agriculture.