The genes are passed from parent to child and greatly increase the risk of a tumour forming.
Researchers from the University of Oxford and the Institute of Cancer Research, London, scanned the genes of 20 people from families with a strong history of bowel cancer.
They found everyone who had a faulty POLE or POLD1 gene developed bowel cancer or had a precancerous growth in the bowel.
The two genes are so-called 'dominant' genes, where only one faulty copy needs to be inherited for someone to be at a high risk of developing bowel cancer.
Researchers looked for the faults in almost 4,000 people with bowel cancer and 6,700 without the disease. Neither of the faults were found in people without bowel cancer, while 12 people with the POLE gene were found in the bowel cancer group and one person had a POLD1 gene fault.
The POLD1 fault was also found to increase the risk of getting womb cancer and possibly brain tumours with seven people in the study being diagnosed with womb cancer and one developing two brain tumours.
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"There are some families where large numbers of relatives develop bowel cancer but who don't have any of the known gene faults that raise the risk of developing the disease," said lead researcher Ian Tomlinson from the University of Oxford.
"These two faults are rare, but if you inherit them your chance of bowel cancer is high. By testing people with a strong family history of the disease for these faults, we can identify those who are at high risk and try to prevent the disease by using colonoscopy and other methods," Tomlinson said in a statement.
POLE and POLD1 are involved in scanning and repairing damage to DNA, removing incorrect sequences from the DNA chain. Without these genes, affected individuals build up damage in their DNA which can cause bowel cancer.
"Uncovering gene faults like these two is extremely important, as inherited susceptibility plays a role in the development of about a third of all cases of colorectal cancer," study co-leader Professor Richard Houlston said.
"This is one of the most important discoveries in bowel cancer genetics in years. It should allow us to manage families affected by inherited bowel cancer much more effectively, and it offers new clues for the prevention or treatment of all forms of the disease," he said.
The study was published in Nature Genetics.