The birds were blasted with an air rifle as they roosted in trees after environmental health officers had tried in vain to capture them alive for four months.
The killings upset some local people who had given them names and enjoyed feeding them with leftover food, grain and pieces of bread.
The cockerels are believed to have been abandoned by their former owner last year on the quayside beside the River Waveney at Beccles, Suffolk.
But while some locals considered them pets, other residents claimed that they were being kept awake by the cockerels crowing as early as 4am.
Waveney Council decided that the birds were a nuisance and started using humane methods to try and capture them in June.
three of the birds managed to avoid capture and started roosting even higher in trees at a height of 25ft to 30ft so they could not be reached.
A decision was finally taken to use a council sharpshooter with an air rifle and torch to blast the birds out of the trees as they roosted.
A local resident who did not wish to be named, described the council's actions as 'disgusting and despicable'.
He added: 'It is really cruel, and a lot of people are very angry about this. Those chickens were pets to a lot of people who fed them. They did no harm whatsoever.'
James Howes, whose mother lives nearby, said: 'I am horrified. Those chickens have been there for years. They could have at least dropped a letter through people's doors to explain what they were doing.'
Andrew Reynolds, the council's principal environmental health officer, said the cockerels had been abandoned illegally and the council had received complaints about noise.
He added: 'This left us with little option but to intervene for the benefit of the health of the community.
'The environmental health team took steps immediately to catch and relocate the cockerels, and the majority of the birds were successfully re-homed without a great deal of fuss.
'However, the remaining cockerels began roosting higher in trees in order to evade capture, prompting us to use a variety of humane methods to capture the birds in order that they could be relocated in a more appropriate environment.
After four months of sustained effort, we exhausted all methods of live capture and exceptional steps were taken to deal with the last three cockerels, which were continuing to cause an unreasonable disturbance.
'We reluctantly took the decision to remove the remaining three by more vigorous means, and our team made the difficult decision to dispatch three cockerels humanely by shooting them. With the successful completion of this, we believe the noise problem is now over.'
Mr Reynolds said the council would consider taking legal action against any residents feeding cockerels which returned to the area.
A council spokeswoman added: 'We first became aware of the cockerels earlier in the summer. We were told they had been dumped a year or so earlier.
'We have no idea who dumped them. We appealed for the owner to come forward in a front page article in the local newspaper six-weeks-ago, but got no response.
'Ten of the cockerels were captured and re-homed by being integrated into chicken populations elsewhere.
'The number of complaints we received is confidential - but we have a duty to respond to noise complaints.
'We believe there are still some hens living wild in the area - but they are not an issue for us and no action is being taken to capture them because they do not make a noise.'