The genetic architecture of resistance for witches’ broom disease of cacao (WBD) was reexamined in an F2 population (Sca-6 × ICS-1), addressing symptom-specificity and possible genetic basis for the differences in disease scores from terminal and cushion brooms. A high-density genetic linkage map was constructed with 494 individuals and 2968 SNPs, obtaining 10 linkage groups comprising 1595 centiMorgans. The trees were evaluated under field conditions with high WBD pressure from 2015 to 2019, with low spatial autocorrelation tested by Moran’s I. Five WBD symptoms and one tree growth trait were mapped, resulting in 23 minor-effects QTLs, primarily arranged in clusters and distributed in all linkage groups except 4 and 6, indicating that WBD has a polygenic inheritance. Terminal and cushion brooms shared a genomic region in linkage group 9, suggesting pleiotropy. In these conditions, the ICS-1 grandparent contributed with more QTLs than Sca-6 to WBD resistance, indicating that the resistance pattern has changed and confirming the susceptible parent’s importance. Few QTLs were identified in the same or proximal loci comparing the 5-year, annual, or biennial periods. Several candidate genes such as glutathione peroxidases, threonine-serine receptors, and endochitinases were potentially associated with WBD resistance. These findings strongly suggest that WBD resistance is more complex than previously postulated, and future directions are presented and suggested to investigate further and improve the insights into WBD resistance.