Edson Buddle got the visitors off the mark after nine minutes in front of 8,142 spectators at the Stadion Stozice following an error from Slovenian defender Darijan Matic who was punished after losing the ball on 20 metres.
However, Clint Dempsey put the United States back in control after 41 minutes and two minutes later the Americans won a penalty after Marko Suler fouled Dempsey with AZ Alkmaar's Jozy Altidore stepping up to slot home the third.
Slovenia pushed forward after the break, threatening Howard three times in as many minutes before Matavz reduced the deficit with his second goal after 61 minutes.
But despite their best efforts the hosts could not give new coach Slavisa Stojanovic a win in his first game in charge after taking over from Matjaz Kek following the side's unsuccessful UEFA EURO 2012 qualifying campaign.
"I was much more satisfied in the second half, in the first half we were timid and lacked structure. In the second half we made some essential repairs, we deserved a goal more," said Stojanovic.