Bain got the bonus despite his involvement in the May 2011 sale being described as “limited”.
A lawyer from Sir David Murray’s own Murray Group also got a £160,000 payout.
The evidence today emerged at Whyte’s trial at the High Court in Glasgow.
The 46 year-old denies a charge of fraud and a second allegation under the Companies Act in connection with his takeover.
Michael McGill – a key adviser to Sir David and a former Rangers director – was giving evidence for a third day.
Whyte’s QC Donald Findlay today quizzed the accountant on who received bonuses “for the Rangers sale being concluded”.
Mr McGill confirmed “two individuals” - then chief executive Bain and Murray Group solicitor David Horne.
Mr Findlay then pushed him on what was paid.
Mr McGill said £360,000 was given to Bain and £160,000 to Horne.
The QC then asked: “£360,000 for what?”
The witness: “He had a long standing arrangement with the Murray Group entered into some years before.”
Mr Findlay: “Did he do anything to help the sale of Rangers to the Whyte group?”
Mr McGill: “I won’t comment if he helped or not. His role, as a whole, was limited, but there was an agreement from years before.”
It was previously heard how Bain had once been given a new contract with a 39-month notice period.
The jury was earlier told how Sir David – as part of his sale – had wanted £5m per year for four years to be invested in the playing squad.
Mr Findlay today claimed £5m “would not get you Messi’s left foot”.
The QC: “The economic reality is that it is not going to make any difference.”
Mr McGill: “I don’t know if I am qualified to say that £5m will make a difference to the football team.”
Mr Findlay said it was “a figure plucked out of the ether” and “a bit of PR window dressing”.
The trial, before Judge Lady Stacey, continues.