Dino Maglio, 35, is suspected of carrying out or attempting similar assaults on up to 15 other women he met through the popular travel site.
On the opening day of a trial which has reignited longstanding safety concerns surrounding the portal, the prosecution said he should go to jail for seven years and four months for the alleged assault on the Australian minor.
As most of the facts of the case are uncontested, it is being dealt with under closed-door, fast-track procedures which mean a verdict could be announced at the end of the next one-day hearing, which was scheduled for April 14th.
Lawyers representing the interests of the victim requested damages of €250,000 for her and a further €50,000 for the trauma suffered by her mother, who also stayed at Maglio's apartment in Padua, near Venice, on the night of the March 2014 attack.
The Italian Ministry of Defence, which is Maglio's employer, is seeking damages of €936,000 - one euro for every citizen in the province of Padua.
Maglio is charged with raping a minor with the aggravating circumstance of having administered a narcotic without her knowledge.
According to the prosecution's account, the girl, who had stayed up chatting to Maglio after her mother and younger sister had gone to bed, was given a drink he had spiked with tranquilisers of a type which have featured regularly in date-rape cases thanks to their ability to trigger confusion, weakness and amnesia in people taking them.
When the mother woke in the morning, she discovered her daughter in Maglio's bed without her underwear and in a state of extreme lethargy.
Arrested after the family filed charges in Venice, Maglio admitted having spiked the girl's drink and to having sexual intercourse with her while she was under the influence but claimed the sex had been consensual.
Police confiscated a stock of 40 'Tavor' pills at his apartment. Tavor is the Italian brand name for Lorazepam, a powerful anti-anxiety drug.
Couchsurfing is a social networking site that puts travellers in touch with hosts who are willing to put them up and show them around their hometowns for free.
The site's declared aim is "a world made better by travel and travel made richer by connection". But its model has been criticised because of previous incidents of travellers being attacked by hosts they know nothing about.
Maglio is expected to face further cases once prosecutors complete their examination of statements made by 15 other women who say they were drugged sexually assaulted or both by the policeman, who used the fake name "Leonardo" to present himself as an amiable and generous host.
The women include nationals of Canada, the Czech Republic, Germany, Hong Kong, Poland, Portugal and the United States. Most of their testimonies were handed to police following a investigation by journalists at the Investigative Reporting Project Italy (IRPI).
After his initial arrest, Maglio was placed under house arrest and suspended from the Carabinieri, a police force which is a branch of the Italian army.
By that stage, complaints about his conduct had begun to circulate online and his Couchsurfing account had been suspended by the site's safety team.
He was, however, able to re-register under a different alias and resumed his attempts to lure women.
Police discovered what he was up to and a raid found him in the company of two women, an Argentinian and an Armenian who showed symptoms of having been drugged.
Only then was he placed in pre-trial custody.