Sugar beet (Beta vulgaris ssp. vulgaris), a key crop for sugar production, faces significant yield losses by the green peach aphid Myzus persicae (Sulzer) and black bean aphid Aphis fabae (Scop.) as well as the transmission of virus by these aphids. The restriction on the use of neonicotinoids in Europe has intensified this problem, emphasizing the urgent requirement for breeding resistant crop varieties. This study evaluated sugar beet germplasm for resistance against these two aphid species. We investigated the performance and feeding behavior of both species on 26 sugar beet genotypes, using leaf disk bioassays and electropenetrography studies. Additionally, whole plant bioassays and semi-field experiments were carried out with M. persicae. Our findings demonstrate the presence of temporal resistance against both aphid species in the primary sugar beet gene pool. We also found that carrying the beet yellows virus (BYV) enhanced the aphids’ performance. Different plant defense mechanisms were involved: resistance against M. persicae primarily occurred prior to the stylet reaching the phloem, particularly in sugar beet line G3. While resistance against A. fabae turned out to be predominately phloem-located. A high incidence of black stomach symptoms in aphids, exceeding 85% across all genotypes, signified a general incompatibility between sugar beet and M. persicae. In conclusion, sugar beet resistance against aphids involved different mechanisms and was aphid-specific. The identification of these mechanisms and interactions represents a crucial milestone in advancing the breeding of sugar beet varieties with improved resistance.