The Ashkenazi Jews (AJ) are a population isolate sharing ancestry with both European and Middle Eastern populations that has likely resided in Central Europe since at least the tenth century. Between the 11th and 16th centuries, the AJ population expanded eastward leading to two culturally distinct communities in Western/Central and Eastern Europe. Our aim was to determine whether the western and eastern groups are genetically distinct, and if so, what demographic processes contributed to population differentiation. We used Approximate Bayesian Computation to choose among models of AJ history and to infer demographic parameter values, including divergence times, effective population sizes, and levels of gene flow. For the ABC analysis, we used allele frequency spectrum and identical by descent-based statistics to capture information on a wide timescale. We also mitigated the effects of ascertainment bias when performing ABC on SNP array data by jointly modeling and inferring SNP discovery. We found that the most likely model was population differentiation between Eastern and Western AJ ∼400 years ago. The differentiation between the Eastern and Western AJ could be attributed to more extreme population growth in the Eastern AJ (0.250 per generation) than the Western AJ (0.069 per generation).