The BV1 gene of the bipartite Begomovirus genome encodes a nuclear shuttle protein (NSP) that is also an avirulence determinant in common bean. The function of the NSP of two common bean-infecting bipartite begomoviruses, Bean dwarf mosaic virus (BDMV) and Bean golden yellow mosaic virus (BGYMV), was investigated using a series of hybrid DNA-B components expressing chimeric BDMV and BGYMV NSP, and genotypes of the two major common bean gene pools: Andean (cv. Topcrop) and Middle American (cvs. Alpine and UI 114). BDMV DNA-A coinoculated with HBDBG4 (BDMV DNA-B expressing the BGYMV NSP) and HBDBG9 (BDMV DNA-B expressing a chimeric NSP with the N-terminal 1 to 42 amino acids from BGYMV) overcame the BDMV resistance of UI 114. This established that the BDMV NSP is an avirulence determinant in UI 114, and mapped the domain involved in this response to the N-terminus, which is a variable surface-exposed region. BDMV DNA-A coinoculated with HBDBG10, expressing a chimeric NSP with amino acids 43 to 92 from BGYMV, was not infectious, revealing an essential virus-specific domain. In the BGYMV background, the BDMV NSP was a virulence factor in the Andean cv. Topcrop, whereas it was an avirulence factor in the Middle American cultivars, particularly in the absence of the BGYMV NSP. The capsid protein (CP) also played a gene pool-specific role in viral infectivity; it was dispensable for infectivity in the Andean cv. Topcrop, but was required for infectivity of BDMV, BGYMV, and certain hybrid viruses in the Middle American cultivars. Redundancy of the CP and NSP, which are nuclear proteins involved directly or indirectly in viral movement, provides a masking effect that may allow the virus to avoid host defense responses.