The Woodlands fighter outpointed defending champion Gamal Yafai in Manchester to claim a major title at a third different weight.
Cunningham downed Yafai three times in the first half of the fight but the former amateur stand-out produced a gallant recovery in the later rounds to keep the pressure on.
The damage had been done however, with Cunningham claiming a unanimous decision, with one scorecard reading 115-110 and two others a surprisingly narrow 114-111.
The 31-year-old - who held the English and Commonwealth titles at bantamweight plus the Commonwealth featherweight crown - took the fight on three weeks’ notice and was rated a 12/1 outsider by some bookmakers on the night.
But he showed his pedigree and determination to consistently hurt Yafai, who walked onto the southpaw’s straight left hand on multiple occasions.
The high energy contest kicked into a higher gear in the second half, with Cunningham surviving a relentless attack by Yafai only to finish the fight the stronger of the two, leaving little doubt on the outcome.
“I’ve had setback after setback,” Cunningham said. “We’ve started from nothing, from the bottom.
“Everything has been on the road. We’ve done it the hard way. Old school titles, no Mickey Mouse titles.
“Three weight major champion and I must be one of the most underrated fighters in Britain.
“I’m always written off, always. And now I think I’ve finally proven myself.”
Cunningham’s victory means Doncaster now has champions at British (Maxi Hughes), European and world (Terri Harper) level.