Chester Nez, 93, of Albuquerque, New Mexico, had told US media he was "very proud" of his part developing the cipher the Japanese never broke.
It was credited with saving the lives of thousands of US troops in the Pacific.
Nez, who was also a painter, died of kidney failure on Wednesday.
"It saddens me to hear the last of the original code talkers has died," Navajo Nation President Ben Shelly told Reuters, adding he was ordering flags to be flown at half-mast in Nez's honour.
"We are proud of these young men in defending the country they loved using their Navajo language."
Nez was chosen from among 250 Navajos who arrived at the Army base in Arizona for the project. He was in high school at the time of his enlistment and lied about his age.
The code took words from the Navajo language, which was spoken by less than 30 non-Navajos at the time, and matched them to military terms. The Navajo word for turtle became "tank", chicken hawk became "dive bomber" and "our mother" meant America.
About 400 code talkers used the cipher to relay messages sent from field telephones and radios throughout the Pacific. Messages read aloud by the code talkers were immediately destroyed.
"It's one of the greatest parts of history that we used our own native language during World War II," Nez said in 2010. "The Japanese did everything in their power to break the code but they never did."
The Code Talker mission was only declassified in 1968. But the original group received the Congressional Gold Medal in 2001, and the programme was dramatised in the 2002 movie Windtalkers.
After World War 2, Nez volunteered in the Korean War, and retired in 1974 after a 25-year career as a painter at the Veterans Administration hospital in Albuquerque.
Despite difficulties travelling since both of his legs were partially amputated, he loved to tell his story, said Judy Avila, who worked with Nez on his memoir.
"He always wanted to go, he loved meeting people," she said. "And with something like kidney failure, it comes really gradually. At the end, he was really tired."

The Dartmouth College team discovered the insects' communication system and studied females' reactions to the males' songs.
They say the call is likely to have evolved from males impersonating hunting bats and startling females.
Females' shuddering response appears to allow males to locate a mate.
Close examination of females' nervous systems suggested that this shudder evolved from a startle reflex, the researchers say.
The findings are published in the journal Current Biology.
Lead researcher Prof Hannah ter Hofstede investigated this unusual insect duet after a colleague presented some recordings of the insects' particularly high frequency chirps.
"It struck me as very strange that these crickets would use such high frequencies for mating purposes," the scientists said.
Other cricket species avoid sounds at these frequencies, which are similar to the sounds that bats make when navigating and hunting.
Prof ter Hofstede used playback experiments - playing males' songs through speakers - to test females' reaction to the high, bat-like chirps.
"I expected the females to walk to the speaker, because this is the usual behaviour for female crickets, but they did not do this - [they instead] made a small jerking motion after each male call," she explained.
"From many observations of males and females together, I noticed that it was always the male walking to the female when she produced these vibrational signals."
Further study revealed that the male calls also triggered activity in a nerve cell known to be responsible for triggering escape behaviour in crickets.
This, along with careful tracking of the cricket evolutionary tree, led Prof ter Hofstede and her colleagues to conclude that what is now a mating song and dance routine originated from a reflex startled "jump".
This, the scientists say, is an example of "how communication systems can change over evolutionary time.
"And that even something as unlikely as a reflex response to a predator can be the origin for a new communication signal."
The last of the 29 Navajo Americans who developed a code with their native language to encrypt military messages in World War 2 has died.
[NEXT_CONCEPT]
Scientists have discovered that the chirps of some crickets could be a cunning way to "startle" potential mates into revealing their location.