Conjugation allows plasmids to move between bacterial species, decoupling plasmid survival from host survival. However, genomic and experimental evidence indicates that many conjugative plasmids are restricted to particular host lineages despite broad theoretical host ranges. Using 4,281 plasmids from an epidemiologically coherent sample of 1,739 Escherichia coli bloodstream infection isolates, we quantify the host-lineage associations of 30 plasmid backbones and assess how these associations structure plasmid co-occurrence. First, we find that host-lineage restriction is strongest for conjugative backbones and increases with plasmid size. Comparison with global plasmid diversity shows that the most host-lineage restricted backbones remain restricted beyond the studied population, whereas the least restricted backbones span an average of 7 host species. We then demonstrate that host-lineage restriction shapes plasmid co-occurrence: backbone pairs with shared host lineages co-occur more frequently than expected. Next, we find that direct plasmid–plasmid associations are rare, suggesting that most plasmid communities coexist opportunistically. Finally, we show that host-lineage restriction of conjugative backbones, together with specificity in conjugative–mobilisable transfer, drives the clustering of mobilisable plasmids. Collectively, our findings reframe conjugation as a mechanism that promotes within-lineage persistence and local plasmid community structure, with potentially important consequences for the accumulation of resistance and virulence determinants.