Dubbed "mini-Leicester" by local media in a salute to last season's surprise English champions, IFK Mariehamn from the Aland Islands capital - population 11,500 - clinched the title with a 2-1 win over Tampere Ilves.
HJK Helsinki, 27-times champions, finished three points behind after they ended the season with a 0-0 draw against last year's champions SJK Seinajoki.
"I still can't believe this is true. I just cried a lot on the pitch," IFK goalkeeper Walter Viitala told Finnish daily Helsingin Sanomat. "I made my mother proud today."
Jamaican international Dever Orgill said their success was built purely on teamwork.
"We live just like a family, we have each other's back at all times ... it's been a great team work, nothing individual," he told public broadcaster YLE.
Mariehamn city said it would organise a celebration in its main square on Monday evening.
IFK Mariehamn spent some 1.2 million euros in the league this year, compared to HJK's 4 million.
Finland's national side have never qualified for the finals of a major international tournament and dropped to their lowest ranking of 101st this month.
Analysts have pointed to a strong focus on ice hockey as the major reason for the lack of football success in the nation of 5.5 million.
(Reporting by Jussi Rosendahl; Editing by Peter Rutherford)
