Stokes, 27, allegedly told a bouncer with a gold tooth and tattoos: "You look like a c***" when he "lost control" on a night out in Bristol.
Bristol Crown Court heard Stokes had started mocking “the camp behaviour” of a group of gay men outside Mbargo nightclub.
Jurors were told the doorman became concerned after seeing Stokes flick his cigarette butt at one of the men’s heads – causing teammate Alex Hales to interject.
Stokes, 27, is jointly charged with affray with Ryan Ali, 28, and Ryan Hale, 27, following the alleged brawl on September 25 last year.
He allegedly knocked Hale unconscious before doing the same to Ali – fracturing his eye socket – after he "started to attack with revenge, retaliation or punishment in mind".
Ali, who works for the emergency services, and Hale had been out separately from Stokes, who had returned to the club at around 2.08am.
The court heard when Stokes and Mr Hales were told the club was closed, Stokes said: “Will 60 quid get us in?”, which he upped to £300 when bouncer Andrew Cunningham refused.
It was said Stokes then told Cunningham: “Look at the state of your teeth, they make you look like a c***.”
Stokes also said Cunningham’s tattoos were s***, the jury heard.
Prosecutor Nicholas Corsellis told jurors “openly gay” Kai Barry and William O’Connor then left the club and chatted to Stokes and Alex Hales.
He added: "Mr Cunningham observed Mr Stokes's behaviour towards them. He noted that he was mimicking their voices and mannerisms in what he described as 'a derogatory way' thereby making fun of their camp behaviour.
"The CCTV footage, which does not have audio, suggests that sort of behaviour with Mr Stokes copying hand gestures made by the men."
Cunnigham then saw Stokes flick a cigarette towards the men – prompting him to say: 'If you want to start on anyone, start on me'.
"Alex Hales asked why Mr Cunningham had become annoyed and when told by him that Stokes had flicked a cigarette at one of the men, he said 'Stokesy… don't do that'."
CCTV then shows Ali and Hale leaving the club and chatting to Barry and O’Connor before the foursome walk off.
Mr Corsellis said it showed Mr Barry touching Ali inappropriately to his groin area, before returning and trying to take his arm.
"Mr Ali responds by pushing Mr Barry away, albeit with no significant force," he told the jury.
He told jurors it would be an issue for them to decide whether the interaction between the men had simply been "banter or something more sinister".
In the meantime, Stokes shook the hand of a doorman and attempted to do the same with Cunningham – who refused to – which then seemed to enrage Stokes, jurors heard.
Mr Corsellis said: “[Stokes] was clearly frustrated and annoyed. He took to acting in a provocative and offensive way towards Mr Cunningham and then Barry and O’Connor.”
Stokes had been staying in a hotel in Bristol with the England cricket team, while Hale and Ali were out together celebrating a promotion and had never met the cricketer before.
Mr Corsellis told the jury: "In the early hours of the morning of Monday September 25 2017, a fight took place between these three defendants in central Bristol in the area known as the Clifton Triangle.
"They were, the Crown say, all involved in threatening and/or using unlawful violence towards each other. Some participated to a greater extent than others as you will see.
"How precisely it started is only known by the defendants. The violence that erupted could actually have stopped very quickly and it would have remained a relatively minor incident.
"But during the incident Mr Stokes lost his control and started to attack with revenge, retaliation or punishment in mind. Well beyond acting in self defence or defence of another.
"He knocked Mr Hale unconscious and then – after time to pause for thought, to calm – he did exactly the same to Mr Ali.
"Mr Ali received significant injuries, including a fractured eye socket, and required hospital treatment."
Mr Corsellis added: "This was not a trivial moment of unpleasantness. It was a sustained episode of significant violence that left onlookers shocked at what was taking place.
"A bottle was used at the beginning by Mr Ali and a broken street sign brought into the fray towards the end by Mr Hale."
Eyewitnesses told jurors today they saw a group of men being "confrontational" and "acting like football hooligans".
Footage shot by Max Wilson shows a man being punched to the floor, with the court hearing Ali had motioned a bottle towards Alex Hales when Stokes got involved.
The pair are then seen in the video grappling to the ground, with jurors hearing Alex Hales told his teammate: "Stokes, Stokes, that's enough".
Wearing a blue suit and red tie, Stokes was driven to Bristol Crown Court this morning in a silver people carrier this morning.
His wife Claire Ratcliffe, who is mother to Stokes' two children, was also in court to support her husband.
The pair wed in East Brent, near Weston-super-Mare, Somerset, on October 14 last year – less than a month after the alleged affray.
Potential jurors were asked by a judge whether they were "extremely committed" cricket fans who followed either the England or India teams but none put their hands up.
The Durham all-rounder will miss this week’s second Test against India at Lord’s.
Stokes also missed the winter Ashes tour debacle after being arrested — although he was made available for the one-day series in New Zealand despite being charged.
The New Zealand-born Stokes issued his initial not guilty plea by video link from Auckland to Bristol in March.
England Cricket Board officials will be inside the court to monitor proceedings throughout.
He is also expected to be accompanied by a representative of the Professional Cricketers’ Association as well as his legal team.
Stokes this weekend took three vital wickets including India skipper Virat Kohli as England won the first Test by 31 runs.
The trial, expected to last between five and seven days, continues.
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