Allergic disease is very common and carries substantial public-health burdens. We conducted a meta-analysis of genome-wide associations with self-reported cat, dust-mite and pollen allergies in 53,862 individuals. We used generalized estimating equations to model shared and allergy-specific genetic effects. We identified 16 shared susceptibility loci with association P < 5 × 10⁻⁸, including 8 loci previously associated with asthma, as well as 4p14 near TLR1, TLR6 and TLR10 (rs2101521, P = 5.3 × 10⁻²¹); 6p21.33 near HLA-C and MICA (rs9266772, P = 3.2 × 10⁻¹²); 5p13.1 near PTGER4 (rs7720838, P = 8.2 × 10⁻¹¹); 2q33.1 in PLCL1 (rs10497813, P = 6.1 × 10⁻¹⁰), 3q28 in LPP (rs9860547, P = 1.2 × 10⁻⁹); 20q13.2 in NFATC2 (rs6021270, P = 6.9 × 10⁻⁹), 4q27 in ADAD1 (rs17388568, P = 3.9 × 10⁻⁸); and 14q21.1 near FOXA1 and TTC6 (rs1998359, P = 4.8 × 10⁻⁸). We identified one locus with substantial evidence of differences in effects across allergies at 6p21.32 in the class II human leukocyte antigen (HLA) region (rs17533090, P = 1.7 × 10⁻¹²), which was strongly associated with cat allergy. Our study sheds new light on the shared etiology of immune and autoimmune disease.