The weight of the honour – considered the "most prestigious" possible by Aboriginal and Torres Strait Island people – was not lost on the out-going chief.
"I am speechless as it's an extraordinary honour to have this presentation of a traditional possum-skin cloak," Demetriou said.
"I am hugely appreciative of the gesture given to me, and I wish to thank the elders for their generosity and kind words upon my leaving the AFL.
"The AFL is a powerful voice of the community within our country, and the AFL stands for inclusion and diversity and a welcome for all people, no matter their background or beliefs.
"I can only say thank you for such an honour and how humbled I am."
AFL head of diversity Jason Mifsud presented the cloak to Demetriou after working with him for the past six years.
He was joined by three senior people of the Gunditjmara nation, which hails from western Victoria.
Mifsud said he consulted other Aboriginal AFL staff members, players and people of the nation in regards to bestowing the enormous honour on Demetriou.
"He's become a great friend of Indigenous people and through the gifting of the cloak, his children, grandchildren and great grandchildren will also carry that friendship through for many generations," Mifsud told AFL.com.au.
"In more ways than one, it's priceless, and we're rapt that he received it with the gracious nature that he did.
"It's quite significant from a cultural point of view.
"Traditional possum skin cloaks are used for a number of reasons, but ultimately they signify someone's superiority – their strength and courage by way of leadership within the Aboriginal community."
Mifsud said the gesture wasn't only a personal recognition but a collective one.
He also said it was rare for an Aboriginal person to have a cloak bestowed upon them, and "extremely rare" for a non-Aboriginal person to receive it.
"We just felt that given Andrew's on-going commitment, courage and conviction to ensure that Aboriginal people have been included in the game and the game be a representative for the things that can be socially positively changed within Aboriginal and Torres Strait Islander communities warranted that level of recognition," he said.
"In many ways, it's the Aboriginal and Torres Strait Islander communities knighting Andrew for his contribution through football and his own personal dedication to the advancement of Aboriginal aspiration.
"There is probably no greater honour you can have bestowed upon you."