Serious cucumber fusarium wilt (CFW) caused by the pathogenic fungus Fusarium oxysporum f. sp. cucumerinum (Foc) frequently occurs during continuous cultivation. The soil bacteria colonized in Foc hyphosphere are supposed to be related to Foc performance and cucumber health. In the present study, culture-independent approach was used to examine the Foc hyphae-associated bacterial communities in different cucumber cropping systems. It was found that the assembly of Foc hyphae-associated bacterial communities was mainly affected by the continuous cucumber practice followed by the pathogen colonization. Proteobacteria, Actinobacteria and Bacteroidetes accounted for 89–93% of the Foc hyphae-associated bacteria, and their abundance changed along with cucumber growth and Foc presence. The abundance of dominant Achromobacter was driven by cucumber cultivation, while the abundance of Rhizobium increased with continuous cucumber cultivation but decreased by Foc spiking. Bioassay tests of cultivable bacterial strains showed that the proportion of Rhizobium and Achromobacter played a key role in the occurrence of CFW, i.e. decreased Rhizobium and increased Achromobacter in the bacterial mixtures led to the decline of Foc suppression. This study indicates the relationship of Foc hyphae-associated bacterial community and cropping systems, and reveals the roles of some specific assembly of dominant bacteria colonizing Foc hyphae in CFW suppression.