Mr McCulloch, Richard King and his wife Heather died on Saturday in a boating incident on the Riverton bar.
"John was my colleague,friend and mentor," McCulloch Architects director Brent Knight said.
"He was always giving of his time and passionate about his community, and the built environment and designing spaces and buildings that work for people.
"John had a great ability to engage with people and get them excited about the creative process, and has left a big legacy in Southland," Mr Knight said.
Mr McCulloch was proud of his involvement in the design of the Celtic columns in Invercargill centre city and a range of residential and commercial projects, including Stadium Southland, Winton Holy Trinity Church, Te Hikoi Museum and Stewart Island and Wallacetown Community Centres.
Longtime friend and fellow architect, Hamish Wixon remembers his colleague of 30 years, as a "passionate Southlander and a passionate architect in equal measure".
"John was always a great thinker and a great problem solver," he said.
"He was just a fantastic bloke and he did everything with great zeal and approached everything with great enthusiasm."
He was also a great outdoorsman — tramper, sailor and boater.
"I did have great admiration for John for what he had achieved in life and for what he had achieved in practice as an architect. He was a man to be admired."
Bluff Yacht Club member Colin McDonald said Mr McCulloch did a lot in Riverton in the short time he was part of the community and he said he "would leave a huge hole in the place".
"It’s an absolute tragedy."
He had been sailing a long time and he was involved with the public ramp replacement.
"John was a leading light in that", Mr McDonald said.
Mr McCulloch retired to Riverton only a few years ago and was a close friend of Richard and Heather King.
"Richard had such a great way of dealing and communicating with people.
"He had a great way of selling an idea to a team," he said. Simple was the way he liked to get things across.
Deep Cove Outdoor Education Trust Board chairman Mike McManus said Mr King was a person who brought so much value and made things happen by saying "let’s just do it".
"I knew Richard and Heather for many years and did many working bees with them. He’s been an integral part of a team that have executed lots of important projects."
Mr King was honoured with a life membership of the trust a couple of years ago.
"Richard had a lifetime involvement in the community and was just an all-round good bloke," Mr McManus said.
Riverton locals were shocked and saddened by the deaths of the couple.
Mrs King was remembered as "a lovely lady" who, along with her husband Richard, was well-liked and would be missed by the Riverton community.