Optimizing plant nitrogen (N) usage and inhibiting N leaching loss in the soil–crop system is crucial to maintaining crop yield and reducing environmental pollution. This study aimed at identifying quantitative trait loci (QTLs) and differentially expressed genes (DEGs) between two N treatments in order to list candidate genes related to nitrogen-related contrasting traits in tomato varieties. We characterized a genetic diversity core-collection (CC) and a multi-parental advanced generation intercross (MAGIC) tomato population grown in a greenhouse under two nitrogen levels and assessed several N-related traits and mapped QTLs. Transcriptome response under the two N conditions was also investigated through RNA sequencing of fruit and leaves in four parents of the MAGIC population. Significant differences in response to N input reduction were observed at the phenotypic level for biomass and N-related traits. Twenty-seven QTLs were detected for three target traits (leaf N content, leaf nitrogen balance index, and petiole NO3− content), 10 and six in the low and high N condition, respectively, while 19 QTLs were identified for plasticity traits. At the transcriptome level, 4752 and 2405 DEGs were detected between the two N conditions in leaves and fruits, respectively, among which 3628 (50.6%) in leaves and 1717 (71.4%) in fruit were genotype specific. When considering all the genotypes, 1677 DEGs were shared between organs or tissues. Finally, we integrated DEG and QTL analyses to identify the most promising candidate genes. The results highlighted a complex genetic architecture of N homeostasis in tomato and novel putative genes useful for breeding tomato varieties requiring less N input. © The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.

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