Stephen Anthony Hough, 58, is also on trial for the sexual assault and manslaughter of Janet Commins, 15.
Mold Crown Court heard Janet's body was found in a field in Flint on 11 January 1976 by three children playing hide and seek.
One man has already served a sentence after admitting Janet's manslaughter, but he insists he did not kill her.
Prosecutor Mark Heywood QC told the jury Janet died "as a result of her neck and her external airway being compressed and blocked during that sexual assault".
Janet had made plans to go swimming on 7 January, but her mother said she did not look well so could not go.
Jurors were told she left her house without her parents knowing and left them a note saying she would be back by 20:30 GMT.
She left the pool just after 19:30 and told a friend she was heading straight home - jurors heard she was spotted with two boys at about 20:10.
The court heard the boy who reported seeing them said one of them was a thin, fair-haired boy and the other was an older-looking boy aged about 17 and they were laughing and joking with Janet.
Her father Edward Commins reported his daughter missing at about 23:00 that night and her body was found four days later.
The court heard Janet was killed during a sexual assault and there were signs her body had been left lying face down "for some time" before being moved to where it was found.
Mr Hough was questioned at the time as his grandparents' house overlooked the area where Janet's body was concealed.
He said he was stealing petrol from a vehicle in Flint that night and was subsequently fined for the offence.
The jury was told that during the original investigation, a man called Noel Jones, then 18, "told his girlfriend that he had killed a young girl".
He was questioned by police and written statements said he admitted raping Janet and she died during the struggle.
However, in a subsequent statement, he said his friend Michael Orford was with him and he also raped Janet.
Jones denied murder but admitted manslaughter and served six years of a 12-year sentence but no evidence was offered against Mr Orford.
Mr Heywood said: "He [Jones] never challenged the circumstances of his conviction, but he asserts that he always knew that he was innocent and he only confessed due to the pressure that he felt placed upon him at the time.
"The prosecution say that when you have considered all the evidence in this case, there is support for Jones's claim that he was not Janet's killer and, in all the circumstances, you can be sure that Stephen Hough was."
In 2006, a review of the scientific evidence in the case was carried out and DNA from a man was identified from samples taken from Janet's body.
In 2016, Mr Hough's DNA was taken by police in an unrelated matter and a match was found, prompting his arrest.
The trial continues.
A man raped and murdered a schoolgirl 40 years ago before dumping her body on a school field, a court has heard.