How a host’s microbiome changes over its lifespan can influence development and aging. As these temporal patterns have only been described in detail for humans and a handful of other hosts, an important next step is to compare microbiome dynamics across a broader array of host-microbe symbioses, and to investigate how and why they vary. Here we characterize the temporal dynamics and stability of the bumblebee worker gut microbiome. Bumblebees are a useful symbiosis model given their relatively well-understood life history and simple, host-specific gut bacterial communities. Furthermore, microbial dynamics may influence bumblebee health and pollination services. We combined high-temporal-resolution sampling with 16S rRNA gene sequencing, quantitative PCR, and shotgun metagenomics to characterize gut microbiomes over the adult lifespan of Bombus impatiens workers. To understand how hosts may control (or lose control of) the gut microbiome as they age, we also sequenced hindgut transcriptomes. We found that, at the community level, microbiome assembly is highly predictable and similar to patterns of primary succession observed in the human gut. At the same time, partitioning of strain-level bacterial variants among colonies suggests stochastic colonization events similar to those observed in flies and nematodes. We also find strong differences in temporal dynamics among symbiont species, suggesting ecological differences among microbiome members in colonization and persistence. Finally, we show that both the gut microbiome and host transcriptome—including expression of key immunity genes—stabilize, as opposed to senesce, with age. We suggest that in highly social groups such as bumblebees, maintenance of both microbiomes and immunity contribute to the inclusive fitness of workers, and thus remain under selection even in old age. Our findings provide a foundation for exploring the mechanisms and functional outcomes of bee microbiome succession, and for comparative analyses with other host-microbe symbioses.