Industrial waste dumps are rarely colonized by vegetation after they have been abandoned, indicating biological infertility. Revegetation of industrial tailings dumps is thus necessary to prevent wind erosion, metal leaching and has been shown to restore soil functions and ecosystem services. However, little is known about the microbial colonization and community structure of vegetated tailings following the application of restoration technologies. In this study, we investigated the rhizosphere and phyllosphere bacterial communities of a poplar tree plantation within a phytomanagement-based restoration program of a Hg-contaminated site. We used Illumina-based sequencing combined with culture-dependent approaches to describe plant-associated bacterial communities and to isolate growth-promoting bacteria (PGPB) and Hg-resistant bacteria. The genus Streptomyces was highly specific to the root community, accounting for 24.4% of the relative abundance but only representing 0.8% of the soil community, whereas OTUs from the Chloroflexi phylum were essentially detected in the soil community. Aboveground habitats were dominated by bacteria from the Deinococcus-Thermus phylum, which were not detected in belowground habitats. Leaf and stem habitats were characterized by several dominant OTUs, such as those from the phylum Firmicutes in the stems or from the genera Methylobacterium, Kineococcus, Sphingomonas and Hymenobacter in the leaves. Belowground habitats hosted more cultivable Hg-resistant bacteria than aboveground habitats and more Hg-resistant bacteria were found on the episphere than in endospheric habitats. Hg-resistant isolates exhibiting plant growth-promoting (PGP) traits, when used as inoculants of Capsicum annuum, were shown to increase its root dry biomass but not Hg concentration. The N2-fixing and Hg-resistant species Pseudomonas graminis, observed in the poplar phyllosphere, may be a key microorganism for the restoration of industrial tailings dumps.