Bi-directional selection for increased and decreased 56-day body weights (BW56) has been applied to two lines of White Plymouth Rock chickens—the Virginia high (HWS) and low (LWS) body weight lines. Correlated responses have been observed, including negative effects on traits related to fitness. Here, we use high and low body weight as proxies for fitness. On a genome-wide level, relaxed lines (HWR, LWR) bred from HWS and LWS purged some genetic variants in the selected lines. Whole-genome re-sequencing was here used to identify individual loci where alleles that accumulated during directional selection were purged when selection was relaxed. In total, 11 loci with significant purging signals were identified, five in the low (LW) and six in the high (HW) body weight lineages. Associations between purged haplotypes in these loci and BW56 were tested in an advanced intercross line (AIL). Two loci with purging signals and haplotype associations to BW56 are particularly interesting for further functional characterization, one locus on chromosome 6 in the LW covering the sour-taste receptor gene PKD2L1, a functional candidate gene for the decreased appetite observed in the LWS and a locus on chromosome 20 in the HW containing a skeletal muscle hypertrophy gene, DNTTIP1.