Watermelon fruit rind color (RC) and bloom formation (BF) affect product value and consumer preference. However, information on the candidate gene(s) for additional loci involved in dark green (DG) RC and the genetic control of BF and its major chemical components is lacking. Therefore, this study aimed to identify loci controlling RC and BF using QTL-seq of the F2 population derived by crossing ‘FD061129’ with light-green rind and bloom and ‘SIT55616RN’ with DG rind and bloomless. Phenotypic evaluation of the F1 and 219 F2 plants indicated the genetic control of two complementary dominant loci, G1 and G2, for DG and a dominant locus, Bf, for BF. QTL-seq identified a genomic region on Chr.6 for G1, Chr.8 for G2, and Chr.1 for Bf. G1 and G2 helped determine RC with possible environmental effects. Chlorophyll a-b binding protein gene-based CAPS (RC-m5) at G1 matched the highest with the RC phenotype. In the 1.4 cM Bf map interval, two additional gene-based CAPS markers were designed, and the CAPS for a nonsynonymous SNP in Cla97C01G020050, encoding a CSC1-like protein, cosegregated with the BF trait in 219 F2 plants. Bloom powder showed a high Ca2+ concentration (16,358 mg·kg−1), indicating that the CSC1-like protein gene is possibly responsible for BF. Our findings provide valuable information for marker-assisted selection for RC and BF and insights into the functional characterization of genes governing these watermelon-fruit-related traits.