Speciation events often occur in rapid bursts of diversification, but the ecological and genetic factors that promote these radiations are still much debated. Using whole transcriptomes from all 13 species in the ecologically and reproductively diverse wild tomato clade (Solanum sect. Lycopersicon), we infer the species phylogeny and patterns of genetic diversity in this group. Despite widespread phylogenetic discordance due to the sorting of ancestral variation, we date the origin of this radiation to approximately 2.5 million years ago and find evidence for at least three sources of adaptive genetic variation that fuel diversification. First, we detect introgression both historically between early-branching lineages and recently between individual populations, at specific loci whose functions indicate likely adaptive benefits. Second, we find evidence of lineage-specific de novo evolution for many genes, including loci involved in the production of red fruit color. Finally, using a “PhyloGWAS” approach, we detect environment-specific sorting of ancestral variation among populations that come from different species but share common environmental conditions. Estimated across the whole clade, small but substantial and approximately equal fractions of the euchromatic portion of the genome are inferred to contribute to each of these three sources of adaptive genetic variation. These results indicate that multiple genetic sources can promote rapid diversification and speciation in response to new ecological opportunity, in agreement with our emerging phylogenomic understanding of the complexity of both ancient and recent species radiations. Combined VCF for all 29 accessions for chromosome 0Pease_etal_SL2.50ch00.vcf.gzCombined VCF for all 29 accessions for chromosome 1Pease_etal_SL2.50ch01.vcf.gzCombined VCF for all 29 accessions for chromosome 2Pease_etal_SL2.50ch02.vcf.gzCombined VCF for all 29 accessions for chromosome 3Pease_etal_SL2.50ch03.vcf.gzCombined VCF for all 29 accessions for chromosome 4Pease_etal_SL2.50ch04.vcf.gzCombined VCF for all 29 accessions for chromosome 5Pease_etal_SL2.50ch05.vcf.gzCombined VCF for all 29 accessions for chromosome 6Pease_etal_SL2.50ch06.vcf.gzCombined VCF for all 29 accessions for chromosome 7Pease_etal_SL2.50ch07.vcf.gzCombined VCF for all 29 accessions for chromosome 8Pease_etal_SL2.50ch08.vcf.gzCombined VCF for all 29 accessions for chromosome 9Pease_etal_SL2.50ch09.vcf.gzCombined VCF for all 29 accessions for chromosome 10Pease_etal_SL2.50ch10.vcf.gzCombined VCF for all 29 accessions for chromosome 11Pease_etal_SL2.50ch11.vcf.gzCombined VCF for all 29 accessions for chromosome 12Pease_etal_SL2.50ch12.vcf.gzRaw Reads located at NCBI BioProject PRJNA305880http://www.ncbi.nlm.nih.gov/bioproject/305880HQ Alignment in Multisample Variant FormatPease_etal_Tomato29acc_HQ.mvf.gzHD Alignment in Multisample Variant FormatPease_etal_Tomato29acc_HD.mvf.gzLQ Alignment in Multisample Variant FormatPease_etal_Tomato29acc_LQ.mvf.gzHQ Coding Sequence Alignment in Multisample Variant FormatPease_etal_Tomato29acc_HQ_prot.mvf.gzGenome-wide all sample phylogenies from gene regions, 100kb and 1Mb regionsPease_etal_TomatoPhylo_GeneTrees.tar.gzGenome-Wide Concatenated/Coalescent/Consensus PhylogeniesPease_etal_TomatoPhylo_GenomeWideTrees.tar.gzQuartet Gene Trees, D-statistics, and DFOIL results for Figs S4/5Pease_etal_TomatoPhylo_QuartetTreeDstatsDFOIL.tar.gz