Verpakovskis made his debut for Latvia on 9 September 1999 in a 2–1 victory over Greece, scoring in that match. He rose to international prominence as the highest goalscorer for Latvia in their successful UEFA Euro 2004 qualification campaign, with 6 goals in 10 matches. He scored once for Latvia in Euro 2004 and nearly scored what could have been a candidate for goal of the tournament against Germany, dribbling on a weaving run from the half way line and beating four German players. Verpakovskis is regarded as the most popular Latvian footballer having surpassed Marians Pahars as his country's most recognisable player. He is currently the leading all-time top goal scorer for Latvia, with 29 goals (). Verpakovskis was Latvia's top scorer in FIFA World Cup 2006 qualification, UEFA Euro 2008 qualification, as well as the FIFA World Cup 2010 qualification. On September 2013, Verpakovskis won his 100th cap for the Latvian national team in a 1–0 World Cup qualifying defeat to Greece. On 29 May 2014, Verpakovskis played his last international match as Latvia beat Estonia in the semi-finals of the 2014 Baltic Cup. He was symbolically substituted by Edgars Gauračs just 13 minutes into the game and honoured by his teammates, national team's staff and supporters. After his retirement the national team's manager Marians Pahars referred to Verpakovskis as "a national team legend". All in all, internationally Verpakovskis has been capped 104 times for Latvia, scoring 29 goals. He is Latvia's all-time best scorer.