Root-knot nematodes (RKN), particularly Meloidogyne incognita, are among the most damaging and prevalent agricultural pathogens due to their ability to infect roots of almost all crop species, including common bean. The best strategy for their control is through the use of resistant cultivars. However, laborious phenotyping procedures make it difficult to assess nematode resistance in breeding programs. For common bean, this task is especially challenging since little has been done to discover resistance genes or find markers to assist selection. In this study, we performed genome-wide association studies and QTL mapping to explore the genetic architecture and genomic regions underlying the resistance to M. incognita and to identify candidate resistance genes. Phenotypic data were collected by a high-throughput assay, and the number of egg masses and root-galling index were evaluated 30 days after inoculation. Complex genetic architecture and independent genomic regions were associated with each trait according to the Fixed and random model Circulating Probability Unification. SNPs located on chromosomes Pv06, Pv07, Pv08 and Pv11 were associated with the number of egg masses, and on Pv01, Pv02, Pv05 and Pv10 with root-galling. A total of 215 candidate genes were identified, including 14 resistance gene analogs and five differentially expressed in a previous RNA-seq analysis. The histochemical analysis indicated that the reactive oxygen species might play a role in the resistance response. Our findings open new perspectives to improve selection efficiency for RKN resistance in common bean, and the candidate genes are valuable targets for functional investigation and gene editing approaches.