HIV-1 non-B subtype infections have been observed in Belgium since the 1980s. However, subtype B predominates amongst men having sex with men (MSM), whereas other subtypes are mainly associated with sub-Saharan African migrants and heterosexual risk behavior. In the last decade, subtype F1 diagnoses have increased substantially in Belgium, representing 9% of newly diagnosed and therapy-naïve HIV-1 patients linked to care in 2014. In the present study, the Belgian subtype F1 epidemic has been characterized within a global context, where F1 is responsible for <1% of HIV-1 infections. The Belgian AIDS Reference Laboratories collected HIV-1 pol sequences from patients linked to care and sub-subtype F1 was verified using Rega v3 and COMET v1.0 subtyping tools. Concordant F1 sequences were retained from 293 patients, who were diagnosed with HIV-1 between 1988 and 2015. The number of F1 diagnoses increased from three in 2001–2 to 83 in 2013–4. Seventy-seven percent were men, with 52% homosexual, 15% bisexual, and 15% heterosexual contact as the probable transmission route (18% not registered). Belgium was the probable country of infection for 54% of the patients, whereas for 38% this information was not registered. A reference dataset from countries with a high burden of F1 infections or with a potential role in the global origin of sub-subtype F1 was collected from public and private databases and the phylogeny was reconstructed using RAxML and BEAST. These analyses indicate that 190 Belgian F1 sequences, 97% from men, and 72% with homosexual/bisexual risk behavior (17% not registered), belong to a monophyletic group with two sub-clades. Together with a Spanish clade, the Belgian clade is embedded in the Brazilian subtype F1 diversity and probably emerged after single or two migration events from South-America with one dead-end lineage (2 strains) and one actively spreading cluster (188 strains). This study reconstructed the structure of the local HIV-1 F1 epidemic and showed that onward transmission of subtype F1 occurs extensively among MSM. It illustrates the introduction and dissemination of strains in one geographically restricted risk group in which the subtype was previously absent.