Introduction: Apple replant disease (ARD) causes reduced growth and fruit yield and affects orchards and tree nurseries worldwide. A number of pathogens have been consistently identified as causal agents of ARD; however factors affecting disease-severity are not fully understood. Aims: We examined five soils from German tree nurseries and apple orchards featuring different soil characteristics and replant histories. We aimed to link the plant-soil interaction to replant disease severity. Methods: In a greenhouse experiment, young apple plants were grown for eight weeks on untreated and disinfected (control) soils. Growth parameters were recorded to evaluate the severity of ARD. The defence response of the plants was examined by expression analysis of ARD indicator genes (BIS3, B4H and ERF1B) and GC–MS-based detection of phytoalexins. The fungal and bacterial rhizosphere communities were investigated by ITS and 16S rRNA amplicon sequencing, respectively. Results: After eight weeks, ARD symptoms were observed on all soils. Growth depression was highest on soils that had faced intensive apple cultivation and lowest on a soil with only one year of apple cultivation prior to the experiment. These results correlated with increases in the BIS3 expression level and the phytoalexin content in the roots. No bacteria and fungi commonly found in increased abundance in ARD soils were consistently detected in all soils. Conclusions: Replant history influenced disease severity more than soil characteristics. ARD symptoms correlated with BIS3 expression and phytoalexin (PA) formation. PA exudation increased the relative abundance of bacterial genera with the potential ability to degrade phenolic compounds.