Kevin Strickland was freed on Tuesday at the age of 62. He had maintained his innocence since his arrest at 18.
It was the longest wrongful incarceration in state history, but under Missouri law he is not entitled to receive any financial compensation.
So his lawyers launched a GoFundMe page to help with his living expenses.
As of Sunday 16:00 GMT, it had reached $1,511,440.
Lawyers for the Midwest Innocence Project, who worked for months to help free Mr Strickland, praised the more than 27,000 strangers who had donated.
The state of Missouri only compensates prisoners exonerated through DNA evidence, not because of eyewitness testimony, his lawyers said.
"Until the system has changed where the system is failing, the community is stepping in to fix it, to fill the void," said Tricia Rojo Bushnell.
A judge on Tuesday ordered Mr Strickland's immediate release from state custody, after 15,487 days behind bars.
He was sentenced to life in prison without the possibility of parole for 50 years after he was linked to the deadly ransacking of a home in Kansas City on 25 April 1978.
On that night, four assailants shot three people inside the home: Sherrie Black, 22, Larry Ingram, 22, and John Walker, 20.
A fourth victim - Cynthia Douglas, 20 - escaped with injuries after pretending to be dead. On a hunch from her sister's boyfriend, police arrested the teenage Mr Strickland and then reportedly pressured Ms Douglas to pick him out of a line-up.
Mr Strickland told police he had been at home watching television. No physical evidence ever linked him to the crimes.