The discovery of unbranched, monocephalic natural variants was pivotal for the domestication of sunflower (Helianthus annuus L.). The branching locus (B), one of several loci apparently targeted by aboriginal selection for monocephaly, pleiotropically affects plant, seed and capitula morphology and, when segregating, confounds the discovery of favorable alleles for seed yield and other traits. The present study was undertaken to gain deeper insights into the genetics of branching and seed traits affected by branching. We produced an unbranched hybrid testcross recombinant inbred line (TC-RIL) population by crossing branched (bb) and unbranched (BB) RILs to an unbranched (BB) tester. The elimination of branching concomitantly eliminated a cluster of B-linked seed trait quantitative trait loci (QTL) identified by RIL per se testing. We identified a seed oil content QTL linked in repulsion and a 100-seed weight QTL linked in coupling to the B locus and additional unlinked QTL, previously masked by B-locus pleiotropy. Genomic segments flanking the B locus harbor multiple loci for domestication and post-domestication traits, the effects of which are masked by B-locus pleiotropy in populations segregating for branching and can only be disentangled by genetic analyses in unbranched populations. QTL analyses of NILs carrying wild B alleles substantiated the pleiotropic effects of the B locus. The effect of the B locus on branching was masked by the effects of wild alleles at independent branching loci in hybrids between monocephalic domesticated lines and polycephalic wild ecotypes; hence, the B locus appears to be necessary, but not sufficient, for monocephaly in domesticated sunflower.