Identified for its critical role in the development of human speech, FOXP2 is a canonical language gene showing a Mendelian pattern of inheritance. Earlier research proposed a recent selective sweep in Homo sapiens targeting two derived amino-acid changes. However, these substitutions were also found in ancient hominin DNA suggesting that the selective sweep was not unique to modern humans. Here, we comprehensively re-analyze FOXP2 with a high-resolution dataset comprising hundreds of next-generation sequenced genomes from globally distributed human populations. We test for fine-scale selection patterns both within the gene and between various human populations in order to resolve a hypothesis of recent positive selection. Intriguingly, haplotype networks and window-based Tajima’s D calculations indicate balancing selection in African populations. Specifically, we identify in silico three major, common FOXP2 haplotypes segregating in modern humans: two within Africa, and one fixed in individuals whose ancestors underwent the Out-of-Africa migration. These three haplotypes span a narrow intronic region that is significantly (P<0.001) evolutionarily conserved across vertebrates based on PhyloP and Genomic Evolutionary Rate Profiling (GERP) scores. Additionally, this region harbors high-GERP SNPs that are derived in humans compared with chimps and archaic hominins. This region of interest is a statistically significant GERP outlier compared to comparably sized genic windows in the same datasets. Strong evolutionary constraint amongst taxa but variability within Homo sapiens is compatible with this locus having a major functional role unique to humans. We examine the effect that these haplotypes might have on the FOXP2 transcription factor’s function (i.e. production of alternative coding isoforms and/or differential expression of target genes) using data from the CommonMind Consortium, which contains matched SNP array and RNA-seq data obtained from fresh cortical brain tissue from hundreds of ethnically diverse individuals.