Long non-coding RNAs (lncRNAs) have emerged as integral gene-expression regulators underlying plant growth, development, and adaptation. To adapt to the heterogeneous and dynamic rhizosphere, plants use interconnected regulatory mechanisms to optimally fine-tune gene-expression-governing interactions with soil biota, as well as nutrient acquisition and heavy metal tolerance. Recently, high-throughput sequencing has enabled the identification of plant lncRNAs responsive to rhizosphere biotic and abiotic cues. Here, we examine lncRNA biogenesis, classification, and mode of action, highlighting the functions of lncRNAs in mediating plant adaptation to diverse rhizosphere factors. We then discuss studies that reveal the significance and target genes of lncRNAs during developmental plasticity and stress responses at the rhizobium interface. A comprehensive understanding of specific lncRNAs, their regulatory targets, and the intricacies of their functional interaction networks will provide crucial insights into how these transcriptomic switches fine-tune responses to shifting rhizosphere signals. Looking ahead, we foresee that single-cell dissection of cell-type-specific lncRNA regulatory dynamics will enhance our understanding of the precise developmental modulation mechanisms that enable plant rhizosphere adaptation. Overcoming future challenges through multi-omics and genetic approaches will more fully reveal the integral roles of lncRNAs in governing plant adaptation to the belowground environment.