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Abstract Facultative, heritable endosymbionts are found at intermediate prevalence within most insect species, playing frequent roles in their hosts’ defence against environmental pressures. Focusing onHamiltonella defensa, a common bacterial endosymbiont of aphids, we tested the hypothesis that such pressures impose seasonal balancing selection, shaping a widespread infection polymorphism. In our studied pea aphid (Acyrthosiphon pisum) population,Hamiltonellafrequencies ranged from 23.2% to 68.1% across a six‐month longitudinal survey. Rapid spikes and declines were often consistent across fields, and we estimated that selection coefficients forHamiltonella‐infected aphids changed sign within this field season. Prior laboratory research suggested antiparasitoid defence as the majorHamiltonellabenefit, and costs under parasitoid absence. While a prior field study suggested these forces can sometimes act as counter‐weights in a regime of seasonal balancing selection, our present survey showed no significant relationship between parasitoid wasps andHamiltonellaprevalence. Field cage experiments provided some explanation: parasitoids drove modest ~10% boosts toHamiltonellafrequencies that would be hard to detect under less controlled conditions. They also showed thatHamiltonellawas not always costly under parasitoid exclusion, contradicting another prediction. Instead, our longitudinal survey – and two overwintering studies – showed temperature to be the strongest predictor ofHamiltonellaprevalence. Matching some prior lab discoveries, this suggested that thermally sensitive costs and benefits, unrelated to parasitism, can shapeHamiltonelladynamics. These results add to a growing body of evidence for rapid, seasonal adaptation in multivoltine organisms, suggesting that such adaptation can be mediated through the diverse impacts of heritable bacterial endosymbionts.