Background: Congenital gonadotropin (GN) deficiency, a subset of hypogonadotropic hypogonadism (HH), can result from defects at the level of the hypothalamus or the pituitary. It is a hallmark of several clinical entities, including: (i) congenital hypogonadotropic hypogonadism (CHH), further classified into normosmic CHH (nCHH) and Kallmann syndrome (KS); (ii) combined pituitary hormone deficiency (CPHD); and (iii) syndromic forms such as CHARGE syndrome and septo-optic dysplasia (SOD). This study aimed to explore the clinical and genetic overlap across these conditions. Methods: All probands who were recruited from Lausanne University Hospital between 2011 and 2023 with congenital GN deficiency (n=568) underwent detailed phenotyping followed by DNA sequencing. Genetic analysis focused on pathogenic (P), likely pathogenic (LP), and variants of uncertain significance (VUS) within established CHH and CPHD genes. Further, oligogenicity was assessed in the CHH/syndromic HH cohort (n=523) and controls from 1000 Genomes (n=601). Cross-entity genetic overlap among CHH, CPHD, and syndromic GN deficiency was also investigated. Results: The cohort included 276 KS, 247 nCHH, 29 CPHD, and 16 syndromic GN deficiency cases. Cleft lip/palate, dental agenesis, and ear abnormalities were recurrent across all groups. Interestingly, some CPHD and SOD patients exhibited anosmia and a preserved GN response to luteinizing hormone-releasing hormone (LHRH) stimulation, suggesting a hypothalamic component to their HH. Rare variants in CHH genes were identified in 53% of KS probands (40% P/LP, 13% VUS) and 33% of nCHH probands (23% P/LP, 10% VUS). FGFR1, ANOS1, and PROKR2 were most frequently mutated in KS, while GNRHR, FGFR1, and KISS1R predominated in nCHH. Oligogenic inheritance was detected in 15% of CHH cases, with variants in FGFR1 most commonly involved. Importantly, 18% of CHH patients without a molecular diagnosis carried rare variants in genes typically associated with CPHD (e.g., DCHS2, FAT2, CDON in KS; ROBO1, FAT2, DCHS2, KCNQ1 in nCHH). Conversely, variants in CHH-associated genes such as FGFR1, CHD7, and FGF8 were found in patients with CPHD and syndromic GN deficiency. Conclusion: This study reveals significant clinical and genetic overlap among GN deficiency disorders. Key findings include: (i) shared developmental features across CHH, CPHD, and syndromic forms; (ii) evidence of dual hypothalamic and pituitary defects in CPHD based on olfactory testing and LHRH response; (iii) oligogenic inheritance in 15% of CHH patients; (iv) identification of novel candidate CPHD genes (ROBO1, DCHS2, FAT2, KCNQ1) contributing to CHH pathogenesis.