Captain Ernie Els and the Lake Nona team took a 6-4 lead after the first day of competition between professionals from two of Florida's most exclusive country clubs.
Holmes, playing with fellow Isleworth member Nick O'Hern, picked up his ball on the 16th green without putting out, earning a penalty that led to a double bogey.
Lake Nona's Ian Poulter eagled the hole, giving himself and fellow Englishman Justin Rose a sudden four-shot lead in the day's final match. Poulter and Rose won by four shots, firing a 7-under 65 to clinch the first-day lead for Nona.
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Monday was a fourball match play round, where the winner of each match is the team with the lowest 18-hole better ball score.
'I was reading my putt when [O'Hern] putted,' Holmes said in an on-course TV interview, struggling to find an explanation for why he picked up his ball. 'I just assumed he put it in.'
The teams were tied 4-4 after splitting the first four matches.
Australians Stuart Appleby and Robert Allenby secured two points for Isleworth in the first match, beating Els and fellow South African Trevor Immelman by a stroke at 5-under 67.
Isleworth captain Mark O'Meara teamed with John Cook to shoot a 68, beating Ben Curtis and Ross Fisher by two shots to give their team two more points.
But Lake Nona dominated the next two matches.
Graeme McDowell and Peter Hanson shot a 65 to beat Arjun Atwal and Lee Janzen by five strokes and cut Lake Nona's deficit to 4-2. Retief Goosen and Henrik Stenson then knocked off Brian Davis and Charles Howell III by four shots with a 64, squaring the match at 4-4.
Holmes' blunder swung the match in Lake Nona's favor.
The competition, which is being held at Isleworth this year, concludes with a round of fourball singles matches on Tuesday, when 20 more points will be awarded. It takes 15 1/2 points overall to win.
Isleworth, which is normally led by Tiger Woods, holds a 3-2-1 record in the all-time series.