Plants actively respond to their neighbors by altering root placement patterns. Neighbor-modulated root responses involve root detection and interactions mediated by root-secreted functional metabolites. However, chemically mediated root placement patterns and their underlying mechanisms remain elusive. We used an allelopathic wheat model system challenged with 60 target species to identify root placement responses in window rhizobox experiments. We then tested root responses and their biochemical mechanisms in incubation experiments involving the addition of activated carbon and functional metabolites with amyloplast staining and auxin localization in roots. Wheat and each target species demonstrated intrusive, avoidant or unresponsive root placement, resulting in a total of nine combined patterns. Root placement patterns were mediated by wheat allelochemicals and (–)-loliolide signaling of neighbor species. In particular, (–)-loliolide triggered wheat allelochemical production that altered root growth and placement, degraded starch grains in the root cap and induced uneven distribution of auxin in target species roots. Root placement patterns in wheat–neighbor interactions were perception dependent and species dependent. Signaling (−)-loliolide induced the production and release of wheat allelochemicals that modulated root placement patterns. Therefore, root placement patterns are generated by both signaling chemicals and allelochemicals in allelopathic plant–plant interactions.