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Genetic studies have identified substantial non-African admixture in the Horn of Africa (HOA). In the most recent genomic studies, this non-African ancestry has been attributed to admixture with Middle Eastern populations during the last few thousand years. However, mitochondrial and Y chromosome data are suggestive of earlier episodes of admixture. To investigate this further, we generated new genome-wide SNP data for a Yemeni population sample and merged these new data with published genome-wide genetic data from the HOA and a broad selection of surrounding populations. We used multidimensional scaling and ADMIXTURE methods in an exploratory data analysis to develop hypotheses on admixture and population structure in HOA populations. These analyses suggested that there might be distinct, differentiated African and non-African ancestries in the HOA. After partitioning the SNP data into African and non-African origin chromosome segments, we found support for a distinct African (Ethiopic) ancestry and a distinct non-African (Ethio-Somali) ancestry in HOA populations. The African Ethiopic ancestry is tightly restricted to HOA populations and likely represents an autochthonous HOA population. The non-African ancestry in the HOA, which is primarily attributed to a novel Ethio-Somali inferred ancestry component, is significantly differentiated from all neighboring non-African ancestries in North Africa, the Levant, and Arabia. The Ethio-Somali ancestry is found in all admixed HOA ethnic groups, shows little inter-individual variance within these ethnic groups, is estimated to have diverged from all other non-African ancestries by at least 23 ka, and does not carry the unique Arabian lactase persistence allele that arose about 4 ka. Taking into account published mitochondrial, Y chromosome, paleoclimate, and archaeological data, we find that the time of the Ethio-Somali back-to-Africa migration is most likely pre-agricultural. Author Summary The Horn of Africa (HOA) occupies a central place in our understanding of modern human origins. This region is the location of the earliest known modern human fossils, a possible source for the out-of-Africa migration, and one of the most genetically and linguistically diverse regions of the world. Numerous genetic studies over the last decades have identified substantial non-African ancestry in populations in this region. Because there is archaeological, historical, and linguistic evidence for contact with non-African populations beginning about 3,000 years ago, it has often been assumed that the non-African ancestry in HOA populations dates to this time. In this work, we find that the genetic composition of non-African ancestry in the HOA is distinct from the genetic composition of current populations in North Africa and the Middle East. With these data, we demonstrate that most non-African ancestry in the HOA cannot be the result of admixture within the last few thousand years, and that the majority of admixture probably occurred prior to the advent of agriculture. These results contribute to a growing body of work showing that prehistoric hunter-gatherer populations were much more dynamic than usually assumed.