• The development of modern crops typically involves both selection and hybridization, but to date most studies have focused on the former. In the present study we explore how both processes, and their interactions, have molded the genome of the cultivated sunflower, a globally important oilseed. • To identify genes targeted by selection during the domestication and improvement of sunflower, and to detect post-domestication hybridization with wild species, we analyzed transcriptome sequences of 80 genotypes, including wild, landrace, and modern lines of Helianthus annuus, as well as two cross-compatible wild relatives, H. argophyllus and H. petiolaris. • Outlier analyses identified 122 and 15 candidate genes associated with domestication and improvement, respectively. As in several previous studies, genes putatively involved in oil biosynthesis were the most extreme outliers. Additionally, several promising associations were observed with previously mapped QTLs, such as branching. Admixture analyses revealed that all of the modern cultivar genomes we examined contained one or more introgressions from wild populations, with every chromosome having evidence of introgression in at least one modern line. • Cumulatively, introgressions cover approximately 10% of the cultivated sunflower genome. Surprisingly, introgressions do not avoid candidate domestication genes likely because of the re-introduction of branching.