Insect immune defense is not static, and dynamic changes in immunity will not be without ecological and evolutionary consequences. Heterogeneity of environments across space, with an element of continuity across time, can select for environment-dependent plasticity in ecologically relevant traits, including immunity. In bumblebees, a social insect, exposure to infectious diseases fits this scenario. Although these bees are depauperate in immune genes relative to most insects, congruent with predictions relating to their ecology they exhibit the phenomenon of trans-generational immune priming (TGIP). Here, immune experience of mothers matters, with offspring from bacterial challenged mother queens showing elevated antibacterial immune defense. While this system of induced increased investment persisting across generations can't be cost free, consideration of important evolutionary and ecologically relevant costs of TGIP has largely taken a back seat during demonstrations of the phenomenon itself. Gene expression work shows that TGIP bumblebee offspring are ready for a similar pathogen assault to that experienced by their mothers experienced, with a constitutive upregulation of costly defences. While this will have a benefit when offspring are faced with matching parasite environments, it comes at a collateral cost to defense against a mismatched parasite. Intriguingly, this cost may materialize through a reconfiguration of the beneficial microbial community associated with the bumblebee gut. These results show that antibacterial TGIP in bumblebees will have ecologically and evolutionary relevant consequences for host parasite interactions, non-target parasite dynamics, and critical beneficial microbes.