Experts including Cancer Research UK scientists at the University of Oxford compared blood samples from 938 patients with head and neck, oesophageal (gullet) and oropharyngeal cancers with 1,599 people without the disease.
They found that more than a third of those who had oropharyngeal cancers also carried antibodies to one of HPV's key cancer-causing proteins - a protein from the HPV16 virus called E6 - and these antibodies could be detected in patients' blood even in samples taken more than 10 years before the cancer was diagnosed.
By comparison, less than 1% of people without cancer carried the antibodies in their blood.
HPV's E6 protein disables the p53 protein, which is often called the 'guardian of the genome' because it protects cells from DNA damage and cancer development.
Having antibodies against this HPV protein indicates that HPV's cancer-causing processes have been activated before.
Scientists in the Oxford study estimated that around seven in 100 non-smoking women and around 23 in 100 non-smoking men who carry the E6 antibody in their blood will develop oropharyngeal cancer over 10 years.
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But patients with oropharyngeal cancers linked to having the HPV infection were more likely to survive than people whose cancers were not related to the infection. Some 84% of people with the HPV16 antibodies in their blood were still alive five years after diagnosis, compared to 58% of people without them.
HPV is already known to increase the risk of developing cervical, vulval, anal and penile cancers. Girls aged 12-13 in the UK are offered vaccination against the two most common cancer-causing HPV types, HPV16 and HPV18. But it is not yet known whether HPV vaccination could protect against oral HPV infections, or oral cancers.
Dr Ruth Travis, one of the authors of the study and Cancer Research UK scientist at the University of Oxford, said: "These striking results provide some evidence that HPV16 infection may be a significant cause of oropharyngeal cancer."
Around 1,500 people are diagnosed with oropharyngeal cancers each year in the UK, and around 470 people die from this disease.
The HPV virus can spread through oral or genital contact. And people who have had a number of oral sex partners have a higher risk of being infected by the virus, but it is not known if this is the only way the virus can spread.
Sara Hiom, Cancer Research UK director of health information, said: "HPV is an extremely common virus. About eight out of 10 people will be infected with the virus at some point in their lives.
"Practising safer sex may reduce the risk of getting or passing on HPV, but condoms won't stop infections completely.
"If the HPV vaccine can also protect against oral HPV infections and cancers, then it could have a broader potential protective effect, but we don't have enough research yet to tell us. At the moment we know it protects against pre-cancerous changes in the cervix, vulva, vagina and anus, as well as reducing the risk of genital warts. So it's important to reduce inequalities, and to aim for high uptake of the vaccine.
"And more research is needed to understand more about HPV infections in the mouth - how they are spread, how easy it is for the body to get rid of them, and what happens when cancer develops - so that we can learn how to reduce the burden of HPV infection in future."
The study is published in the Journal of Clinical Oncology.