Many economically important crops lack suitable genomic tools and annotations, including avocado (Persea americana). We created a reference genome from the Gwen varietal, which is closely related to the agronomically dominant Hass varietal. We produced a 1,032Mb genome assembly with an N50 of 3.37Mb, and a BUSCO score of 91%. We scaffolded the assembly using a genetic map, which led to 12 pseudo-chromosomes representing 78% of the expected genome size containing 49,450 genes. To investigate the domestication history of avocado, we also compiled a database of 34 resequenced genomes that represented major cultivars and the three botanical races of P. americana. Also, in order to elucidate the heterodichomagous nature of avocados, we took into consideration an even distribution of both flowering types in our selection of accessions. Our analyses were consistent with a separate domestication event for each race, and we estimated early genetic separation, with the Mexican race diverging from the Lowland (formerly known as 'West Indian') and Guatemalan races >1 million years ago. We identified putative targets of selective sweeps within domestication; within the Guatemalan race, putative candidate genes were enriched for fruit development and ripening, while the Lowland and Mexican races shared more putative domestication genes than expected at random. We also investigated divergence between races and especially between heterodichomagous flower types. The latter identified genes enriched for functions in pollination, flower development, circadian rhythm and photoperiodism. Genes in regions of divergence were also enriched for GO functions in pollination and flower development.