Background Backgrounding (BKG), the stage between weaning and finishing, significantly impacts feedlot performance in beef cattle; however, the contributions of the rumen microbiome to this growth stage remain unexplored. A longitudinal study was designed to assess how BKG affects rumen bacterial communities and average daily gain (ADG) in beef cattle. At weaning, 38 calves were randomly assigned to three BKG systems for 55 days (d): a high roughage diet within a dry lot ( DL, n=13); annual cover crop within a strip plot ( CC, n=13); and perennial pasture vegetation within rotational paddocks ( PP, n=12), as before weaning. After BKG, all calves were placed in a feedlot for 142 d and finished with a high energy ration. Calves were weighed periodically from weaning to finishing to determine ADG. Rumen bacterial communities were profiled by collecting fluid samples via oral probe and sequencing the V4 region of the 16S rRNA bacterial gene, at weaning, during BKG and finishing.Results Rumen bacterial communities diverged drastically among calves once they were placed in each BKG system, including sharp decreases in alpha diversity for CC and DL calves only ( P < 0.001). During BKG, DL calves showed a substantial increase of Proteobacteria, Succinivibrionaceae family ( Ruminobacter, Succinimonas ) (P<0.001), which also corresponded with greater ADG ( P < 0.05). At the finishing stage, alpha diversity decreased dramatically and Proteobacteria bloomed for all calves, with no previous alpha or beta diversity differences being retained between groups. However, at finishing, PP calves showed compensatory ADG, particularly greater than that in calves coming from DL BKG, who showed the lowest ADG ( P = 0.02). Microbe network dynamics and network traits related to centrality, connectivity, degree, number and strength of microbe-microbe interactions in the rumen were predictive of ADG during BKG and finishing.Conclusions Assessing rumen bacterial community composition, and particularly microbemicrobe interactions under different BKG systems may be useful in predicting growth performance in beef cattle. These findings underscore the importance of early post weaning stages as potential targets for feeding interventions that can modulate the rumen microbiome to enhance life-long productive performance in beef cattle.