Background Ticks transmit pathogens of medical and veterinary importance and are an increasing threat to human and animal health. Assessing disease risk and developing new control strategies requires identifying members of the tick-borne microbiota as well as their temporal dynamics and interactions. Methods Using high-throughput sequencing, we studied the Ixodes ricinus microbiota and its temporal dynamics. 371 nymphs were monthly collected during three consecutive years in a peri-urban forest. After a Poisson lognormal model was adjusted to our data set, a principal component analysis, sparse network reconstruction, and differential analysis allowed us to assess seasonal and monthly variability of I. ricinus microbiota and interactions within this community. Results Around 75% of the detected sequences belonged to five genera known to be maternally inherited bacteria in arthropods and to potentially circulate in ticks: Candidatus Midichloria, Rickettsia , Spiroplasma , Arsenophonus and Wolbachia . The structure of the I. ricinus microbiota varied over time with interannual recurrence and seemed to be mainly driven by OTUs commonly found in the environment. Total network analysis revealed a majority of positive partial correlations. We identified strong relationships between OTUs belonging to Wolbachia and Arsenophonus , evidence for the presence of the parasitoid wasp Ixodiphagus hookeri in ticks. Other associations were observed between the tick symbiont Candidatus Midichloria and pathogens belonging to Rickettsia . Finally, more specific network analyses were performed on TBP-infected samples and suggested that the presence of pathogens belonging to the genera Borrelia , Anaplasma and Rickettsia may disrupt microbial interactions in I. ricinus . Conclusions We identified the I. ricinus microbiota and documented marked shifts in tick microbiota dynamics over time. Statistically, we showed strong relationships between the presence of specific pathogens and the structure of the I. ricinus microbiota. We detected close links between some tick symbionts and the potential presence of either pathogenic Rickettsia or a parasitoid in ticks. These new findings pave the way for the development of new strategies for the control of ticks and tick-borne diseases.