The aim of this study was the improvement of a genetic map of the F₁ population from the cross between the fungus-resistant grapevine cv. “Regent” and the susceptible cv. “Lemberger” and its use to localize factors affecting pathogen resistance and leaf morphology. To construct an integrated map combining the information from both parental meiotic recombination frequencies co-dominant microsatellite markers were employed. Resistance gene analog (RGA)-derived and sequence characterized amplified regions (SCAR) markers correlated with powdery and downy mildew resistance were additionally mapped. The new integrated map contains 398 markers aligned along 19 linkage groups, covers a total length of 1,631 cM and shows an average distance between markers of 4.67 cM. One hundred and twenty-two microsatellite markers were newly mapped. This genetic map was used to localize QTLs (quantitative trait loci) conferring resistance to powdery and downy mildew pathogens transmitted from “Regent”. Factors influencing specific leaf morphology traits were identified in addition. A major QTL for powdery mildew resistance and one major and one minor QTL for downy mildew resistance were detected. Some RGA-derived markers are found co-located in the region covered by the major QTL for resistance to downy mildew hinting at their putative functional relevance. Furthermore, 27 QTLs affecting leaf morphology descriptors were identified. This map is an important tool for grapevine breeding and resistance research.