Rhizosphere functioning depends on plant traits, but the underlying genotypic properties are poorly understood. Wheat has undergone several domestication events combined with genomic hybridization, including the acquisition by Triticum dicoccon (AABB genome) of the D genome from Aegilops tauschii, resulting into bread wheat Triticum aestivum (AABBDD genome). The D genome is likely to modulate the functioning of beneficial wheat-microbe interactions, but data are needed to substantiate this. Here, we tested the hypothesis that genome D is important for soil interactions of wheat with 1-aminocyclopropane-1-carboxylate (ACC) deaminase producers, a key microbial functional group that enhances plant performance by fine-tuning ethylene metabolism in roots. A range of wheat lines from T. aestivum (AABBDD), T. diccocon (AABB) and Ae. tauschii (DD) were compared based on abundance (qPCR on acdS gene marker), diversity (Illumina MiSeq) and potential ACC deaminase activity (colorimetric assays) of ACC deaminase producers in the rhizosphere. Results showed that the abundance of ACC deaminase producers was lower for D-genome wheats than D-negative T. dicoccon at 40 days, but ACC deaminase potential activity in the rhizosphere was lower for D-genome Ae. tauschii and T. aestivum landraces than T. aestivum cultivars (recent and old), while D-negative T. dicoccon was in between. Rhizosphere community structure of Ae. tauschii and T. dicoccon differed from that of T. aestivum, and differences occurred also between various genotype categories of T. aestivum. Overall, the acquisition of the D genome has had a negative impact on the ability of wheat to recruit ACC deaminase producers in soil, but bread wheats resulting from recent breeding displayed improved ACC deaminase activity in the rhizosphere.