McCarthy, who died in Las Vegas last week, was honoured in a Catholic Mass at St Mary's Star of the Sea Church in Sorrento on Thursday morning.
Around 1500 mourners were present, with the crowd spilling out of the church and into a nearby marquee and secondary room, where they watched the service on screens.
Watch a tribute to John McCarthy on CTV in the video above.
His mother Catherine was among five family members who provided moving tributes, which all contained the same theme - how much McCarthy loved life, his family and friends.
Mrs McCarthy said her family had been "overwhelmed and truly humbled" by the amount of support they had received since her son's tragic accident last Monday.
She said John could not have been loved more.
"Our Johnny boy is one of the most extraordinary human beings we have been privileged to know," Mrs McCarthy said.
"His love, kindness, softness, spirituality … he was a very spiritual boy, who we had recently heard prayed for his family every night, and everyone he loved.
"He loved his family with intensity. He was lover and not a fighter, but if you crossed one of his own you were in trouble."
McCarthy had recently been visited in Adelaide, where he moved to at the end of last year after his trade to Port Adelaide, by his parents when his partner Dani went to India to attend a wedding.
Mrs McCarthy recalled how as her son hadn't been able to come home for some time due to football commitments, he had asked for photos of all their housing renovations.
She reflected on that trip to Adelaide, where the roles were reversed and her son decided to look after them instead of the other way around.
"Shane and I arranged to go to Adelaide to look after John. 'As a mother I will look after you, cook your meals and wash your clothes,'," she said.
"We arrived and the house was immaculate, the sheets freshly laundered, towels folded on the end of the bed, flowers in vases, even the bathroom mirror cleaned.
"I said, 'Johnny, you didn't have to clean the house for us, I was coming to look after you.'
"He said, 'I know that mum, but I wanted to look after you, so you could relax and have fun.'"
Among the mourners at the service were AFL CEO Andrew Demetriou and AFLPA CEO Matt Finnis, with representatives from all AFL clubs also present.
Richmond captain Chris Newman, Western Bulldogs captain Matthew Boyd and teammate Daniel Cross, Melbourne's Nathan Jones, Geelong's Tom Lonergan, ex-Collingwood and Gold Coast ruckman Josh Fraser and former Pie Shane O'Bree made the trip down to Sorrento.
Newly appointed Carlton coach and former Collingwood coach Mick Malthouse arrived with his wife Nanette, and coaches including Melbourne's Mark Neeld and Gold Coast's Guy McKenna were also at the service.
Former Port Adelaide coach Matthew Primus, who was responsible for recruiting McCarthy to the club at the end of last season, also attended.
Mrs McCarthy remembered her son as someone who "generated love", and their family as one that didn't use handshakes; "only hugs, kisses and love".
The McCarthys watched their son wear a Collingwood jumper for four years and a Port Adelaide one for the season just gone.
Mrs McCarthy said she hoped her son would be with his former teammates when they played against each other in future years.
"As parents of footballers, we know your trials and tribulations," she said.
"We feel for you in the tough times, knowing that as very young men you are exposed to pressures well beyond your years. You are an exemplary group of men.
"This may not make coaches happy, but when Port Adelaide plays Collingwood, we pray for a draw.
"Whatever the results, we will be cheering for every player out there, and hoping Johnny is helping them. Never play for Johnny, just play with him."
At the memorial service on Thursday morning at Alberton Oval, around 1500 people, including representatives from the Adelaide Football Club and the South Australian Premier Jay Weatherill, were offered John McCarthy badges to wear as a gesture of respect as they arrived.
Once there was no longer room in the main grandstand, seating on the oval itself quickly filled as well.
On a stage with its back to the Power's Alan Scott Headquarters and next to a framed picture of McCarthy playing this season, Port Adelaide deputy chairman Kevin Osborn described the 22-year-old as "a warrior" and vowed he would never be forgotten.
As the crowd watched the live feed of McCarthy's funeral from Sorrento, there was laughter at stories from his childhood and tears as Smarrelli spoke of their time together.
Collingwood players and officials at Sorrento's St Mary's Star of the Sea Church during the service for John McCarthy.
