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Simple Summary: The tomato leafminer, Tuta absoluta, is a devastating pest moth of commercially important crops like tomato and potato. This moth has developed resistance to insecticides; therefore, novel approaches, like using natural predators, are needed to combat infestations. We explored the use of tropical tent web spiders, Cyrtophora citricola, as biological control agents, as these spiders live in groups and are not cannibalistic, and thus, create large, predator-dense webs. Furthermore, their global range overlaps with regions of moth infestations. In lab settings, we introduced different prey types to small colonies of spiders of varying body sizes and found that spiders were equally efficient at capturing pest moths and easily-caught fruit flies (Drosophila hydei). Larger spiders built larger webs and were better at catching prey. Spiders from southern Spain were large enough to capture pest moths during the tomato growing season, but >50% of spider egg sacs were attacked by egg predatory wasps (Philolema palanichamyi). Cyrtophora citricola spiders, therefore, have the potential to be an effective biological control agent of flying insect pests, at least after growing to medium-sized juveniles, and if wasp infections are controlled, forming part of integrated pest management to defend against pest infestations in the future. Group-living spiders may be uniquely suited for controlling flying insect pests, as their high tolerance for conspecifics and low levels of cannibalism result in large, predator dense capture webs. In laboratory settings, we tested the ability of the facultatively communal spider, Cyrtophora citricola, to control the tomato leafminer, Tuta absoluta; a major pest of tomato crops worldwide. We tested whether prey capture success was affected by spider body size, and whether prey capture differed among T. absoluta, flightless fruit flies (Drosophila hydei), and larger black soldier flies (Hermetia illucens). We found that larger spiders generally caught more prey, and that prey capture success was similar for T. absoluta and easily caught fruit flies, while black soldier flies were rarely caught. We further investigated the seasonal variations in web sizes in southern Spain, and found that pest control would be most effective in the tomato planting and growing season. Finally, we show that C. citricola in Spain have >50% infection rates of an egg predatory wasp, Philolema palanichamyi, which may need controlling to maintain pest control efficacy. These results suggest that using C. citricola as a biological control agent in an integrated pest management system could potentially facilitate a reduction of pesticide reliance in the future. [ABSTRACT FROM AUTHOR]