The genetic architecture of the nitrogen use efficiency (NUE) is complex and has two components, namely NUpE (N uptake efficiency) and NUtE (N utilization efficiency). During the present study, the genetics of NUE and its two components was examined using a bi-parental mapping population comprising 149 recombinant inbreed lines (RILs), derived from a cross between two Indian wheat cultivars, namely HUW468 (high NUE) and C306 (low NUE). The mapping population, two parental genotypes and three check genotypes were evaluated under four different N levels (0, 60, 120, and 180 kg/ha) over three consecutive crop seasons. A genetic map containing a total of 456 SNP loci distributed on 21 linkage groups with a total coverage of 2,571.38 cM was used for QTL analysis. A set of 51 QTLs comprising 25 QTLs for NUE, 18 QTLs for NUpE and 8 QTLs for NUtE were identified; these were distributed on 12 chromosomes (1B, 1D, 2A, 2B, 3A, 4B, 5A, 5B, 5D, 6A, 6D, and 7A). LOD score of these QTLs ranged from 2.52 to 9.27 and the individual QTLs explained phenotypic variation ranging from 6.65% to 22.89%. In addition, 38 digenic epistatic interactions involving 45 E-QTLs were also identified. A total of 737 candidate genes (CGs) were mined from the QTL regions. Most of these CGs were involved in metabolic process, cellular process, catalytic activity etc. In-silico expression analysis showed differential expression of 49 CGs in roots and 34 CGs in shoots under low-N vs sufficient-N in a pot culture experiment. The CGs encoded some of the transcription factors (TFs) and other important proteins having roles in N metabolism, transportation, etc. The QTLs and CGs reported in this study add to the available knowledge and can be successfully utilized for marker-assisted breeding for improvement of NUE traits in wheat.