The present study investigated the linkage between days to flowering (DTF) and Growth Habit (GH) in pigeonpea using QTL mapping, QTL-seq, and GWAS approaches. The linkage map developed here is the largest to date, spanning 1825.56 cM with 7987 SNP markers. In total, eight and four QTLs were mapped for DTF and GH, respectively, harboring 78 pigeonpea orthologs of Arabidopsis flowering time genes. Corroboratively, QTL-seq analysis identified a single linked QTL for both traits on chromosome 3, possessing 15 genes with genic variants. Together, these 91 genes were clustered primarily into autonomous, photoperiod, and epigenetic pathways. Further, we identified 39 associations for DTF and 111 associations for GH through GWAS in the QTL regions. Of these, nine associations were consistent and constituted nine haplotypes (five late, two early, one each for super-early and medium duration). The involvement of multiple genes explained the range of allelic effects and the presence of multiple LD blocks. Further, the linked QTL on chromosome 3 was fine-mapped to the 0.24 Mb region with a LOD score of 8.56, explaining 36.47% of the phenotypic variance. We identified a 10 bp deletion in the first exon of TFL1 gene of the ICPL20338 variety, which may affect its interaction with the Apetala1 and Leafy genes, resulting in determinate GH and early flowering. Further, the genic marker developed for the deletion in the TFL1 gene could be utilized as a foreground marker in marker-assisted breeding programs to develop early-flowering pigeonpea varieties.