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Coevolution is a force contributing to the generation and maintenance of biodiversity. It is influenced by environmental conditions including the scarcity of essential resources, which can drive the evolution of defence and virulence traits. We conducted a long‐term chemostat experiment where the marine cyanobacteriumSynechococcuswas challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. This manipulation of nutrient stoichiometry altered the stability of host–parasite interactions and the underlying mode of coevolution. By assessing the infectivity with > 18 000 pairwise challenges, we documented directional selection for increased phage resistance, consistent with arms‐race dynamics while phage infectivity fluctuated through time, as expected when coevolution is driven by negative frequency‐dependent selection. The resulting infection networks were 50% less modular under N‐ versus P‐limitation reflecting host‐range contraction and asymmetric coevolutionary trajectories. Nutrient stoichiometry affects eco‐evolutionary feedbacks in ways that may alter the dynamics and functioning of environmental and host‐associated microbial communities.