We present an initial exploratory framework, Ancestral Genome Reconstruction (AGR), to automatically infer ‘paleogenomes’ from large comparative datasets. By analyzing 84 extant angiosperm species, we reconstructed 10 key ancestral plant genomes of millions of years old. These reconstructed ancestors were instrumental in (i) estimating when emerged the angiosperms as well as major botanical families as well as ancestral shared whole genome duplication events, (ii) tracing the evolutionary trajectories of ancestral chromosomes as well as genes, especially those that may have driven the emergence of key life history traits (exemplifies with woody vs. herbaceous, aquatic vs. terrestrial, C3 vs. C4 and symbiotic root nodulators vs. non-nodulators species). We demonstrate that these paleogenomes serve as tractable backbones for inter-crop translational research, in delivering though an open access web tool (OrthoViewer) genes that have conserved the same ancestral genomic context favoring the identification of ‘phenologs’ -genes underlying similar phenotypes, traits, or processes across species- exemplified with FUWA for yield components, FLC for flowering time, and DDM1 for DNA methylation. Taken together, this study provides a testable paleogenomics workflow, opening novel avenues to integrate evolutionary genomics data into modern climate-smart breeding and support the agroecological transition.