The adenomatous polyposis coli gene (APC) is one of the earliest driver mutations observed in sporadic cancer. Patients with familial adenomatous polyposis disease (FAP) possess a germline APC mutation at birth leading to hundreds of colonic polyps and eventually a 100% lifetime risk of colorectal cancer. These patients often undergo a total colectomy once their polyp burden is unmanageable; as such, these resected colons are a rich source of histologically normal mucosa, benign, dysplastic, and, on rare occasions, adenocarcinomas. As part of the precancer atlas initiatives we performed whole genome/exome sequencing on 127 independent samples across these different stages of pre-malignant tissue spanning all colon regions from six patients. We characterize the early events driving colorectal cancer development and malignant progression, comparing our findings with existing single polyp multi-region studies of sporadic colorectal cancer and FAP samples. We reveal that spatially separated polyps from the same patient harbor numerous subclonal mutations in common, but evolve independently, consistent with a model of polyclonal origin.