Ashdown House in Forest Row, East Sussex, had an environment where “sexual touching was seen as acceptable”, during almost 25 years of abuse from 1969, the hearing was told.
The latest round of the inquiry – looking at abuse at residential schools – identified Ashdown House as one of its points of focus.
Lead counsel Fiona Scolding QC explained it was a “feeder school for the most significant public schools such as Eton” and with past pupils including “the current Prime Minister”.
Mr Johnson attended the school in 1975 – six years after the first allegations of sexual abuse of it pupils were made.
Ms Scolding told the inquiry: “The regime at the school has been described in the [victims’] accounts as ‘Spartan and unforgiving’.
“The boys who were abused identified a sexualised culture created by the abuse of staff against pupils.
“It was an environment where sexual touching was seen as acceptable and normal.”
Ms Scolding said abuse was disclosed at the time by parents, but that the police were not informed.
She said allegations of sexual abuse had been made against at least seven Ashdown House staff, involving 15 complainants.
Two of those staff have since died and one cannot be found, she said.
Another, Martin Haigh, who taught at the school between 1973 and 1975, is the only person to have been convicted.
Ms Scolding said: “Haigh’s modus operandi would be to repeatedly come into the dormitories where children would sleep, make them stand in a circle naked and ask them to masturbate.
“He would then hang things from their erections, telling them this was a ‘scientific exercise’.
“He would also take photos of these boys.”
She added: “Haigh admitted sexually abusing three boys to the [then] headteacher and left under a cloud in 1975.”
But she said nobody thought to contact the police or refer the matter to the Department for Education.
The hearing was told Haigh admitted sexually assaulting two people and was also found guilty of possession of indecent images of children and taking photos of them.
He was further tried in 2017 and found guilty of 11 child sexual offences, and a further four offences of making indecent images of children against four boys.
He was jailed for 12 years.
Founded in 1843, the 125-pupil Ashdown House School has been owned by the Cothill Educational Trust since 2009.
It is a boarding and day school and now caters for boys and girls aged from five to 13.
A number of other schools will be examined during this tranche of the inquiry, including Chetham’s School of Music in Manchester.
Ms Scolding said: “What comes through clearly is that the sexual abuse perpetrated upon them (pupils) can cause them to feel a sense of shame and guilt, that the abuse was their fault or their responsibility. It plainly was not.
“Sexual abuse, as we know, can leave an indelible scar upon the most resilient of individuals.”
The hearings are expected to last until Friday.