Chronic infections imply that the parasite and the host immune system closely interact for a long time without a fatal outcome. Environmental changes encountered by hosts and parasites, such as coinfections, can deeply affect the stability of this apparent equilibrium. Our study aimed to determine the effect of the infectious environment on the costs and benefits of chronic infection with the gut nematode Heligmosomoides polygyrus in mice. Heligmosomoides polygyrus is known for its capacity to actively interfere with the host immune response by secreting molecules that can dampen immunity. We simulated bacterial coinfection of H. polygyrus-infected CBA-strain mice during the chronic phase of the infection by injecting them with Escherichia coli lipopolysaccharide. We found that infection by H. polygyrus induced only weak costs for the host (in terms of reproductive investment) and was characterized by the upregulation of both Th1 (interferon-γ) and anti-inflammatory (transforming growth factor-β) cytokines, which is favorable to parasite persistence. However, when co-occurring with the simulated bacterial infection, H. polygyrus infection was associated with a pronounced shift toward a pro-inflammatory status, which was deleterious to both the parasite and the host. Our study highlights the dynamic equilibrium reached during chronic infection, where a rapid environmental change, such as a concomitant bacterial infection, can deeply affect the outcome of the host-parasite interaction.