Campylobacter spp. are known for their compact genomes and plastic accessory gene pools that are shaped by recombination, plasmid-mediated horizontal gene transfer, and interspecific introgression. Their host-dependent ecology allows them to act as both animal commensals and human pathogens, which in turn promotes adaptation to antimicrobials and diversification into both host specialist and generalist lineages. We  systemically queried whether accessory-gene frequencies are temporally stable or change directionally, and whether trends reflect shifts in lineage composition or gene-level processes. We built temporal pangenome graphs for Campylobacter coli and jejuni from publicly available genomes of UK isolates spanning approximately over the last 20 years. In C. coli, both population structure and the accessory gene frequencies were close to equilibrium across the study period. In contrast, C. jejuni showed widespread changes in accessory gene frequencies largely decoupled from lineage dynamics, implicating horizontal transfer and selection in maintaining gene frequencies independent of population turnover. Ortholog trajectories revealed allelic replacements in core and essential genes. Further, temporal pangenome trajectories highlighted frequent change in genes involved in the “decoration” arm of protein glycosylation. Finally, we identified cases of negative epistasis among accessory elements in C. jejuni. Temporal pangenome graphs we were used to resolve gene- versus lineage-level forces, and refine models of pangenome evolution. These results inform AMR surveillance and interventions targeting virulence-associated factors through modelling of gene-level evolutionary responses.