Populations of the vegetable pathogen Phytophthora capsici are often highly diverse, with limited gene flow between fields. To investigate the structure of a newly established, experimental population, an uninfested research field was inoculated with two single-zoospore isolates of P. capsici in September 2008. From 2009 through 2012, ≈50 isolates of P. capsici were collected from the field each year and genotyped using five microsatellite loci. The same two isolates were also crossed in the lab. High levels of diversity were detected in the research field, with 26 to 37 unique multilocus genotypes detected each year. Through 2012, genotypic diversity did not decline and no evidence of genetic drift was observed. However, during the 2011 and 2012 growing seasons, four new alleles not present in either parental isolate were observed in the field. Selfing (but not apomixis) was observed at low frequency among in vitro progeny. In addition, evidence for loss of heterozygosity was observed in half of the in vitro progeny. These results suggest that recombination, mutation, and loss of heterozygosity can affect the genetic structure observed in P. capsici populations.