Comprehensive information of a breeding population is a necessity to design promising crosses. This study was conducted to characterize a soft red winter wheat breeding population that was subject of intensive germplasm introductions and introgression from exotic germplasm. We used genome-wide markers and phenotypic assessment to identify signatures of selection and loci controlling agronomic traits in a soft red winter wheat population. The study of linkage disequilibrium (LD) revealed that the extent of LD and its decay varied among chromosomes with chromosomes 2B and 7D showing the most extended islands of high-LD with slow rates of decay. Four sub-populations, two with North American origin and two with Australian and Chinese origins, were identified. Genome-wide scans for selection signatures using F ST and hapFLK identified 13 genomic regions under selection, of which five loci (LT, Fr-A2, Vrn-A1, Vrn-B1, Vrn3) were associated with environmental adaptation and two loci were associated with disease resistance genes (Sr36 and Fhb1). Genome-wide association studies identified major loci controlling yield and yield related traits. For days to heading and plant height, major loci with effects sizes of 2.2 days and 5 cm were identified on chromosomes 7B and 6A respectively. For test weight, number of spikes per square meter, and number of kernels per square meter, large effect loci were identified on chromosomes 1A, 4B, and 5A, respectively. However, for yield alone, no major loci were detected. A combination of selection for large effect loci for yield components and genomic selection could be a promising approach for yield improvement.