In 2008 Berkowitz ran for election as U.S. Representative for Alaska's at-large congressional district, held by scandal-plagued Republican Don Young, who was seeking his 19th term in Congress.

[12][13] Berkowitz entered the race following Palin's resignation in July 2009 and on August 24, 2010, he defeated State Senator Hollis S. French for the Democratic nomination.

Incumbent Republican Governor Sean Parnell defeated Berkowitz and his running mate Diane E. Benson in the November general election, 59% to 38%.

He finished ahead of the rest of the field in the nonpartisan primary on April 7, advancing to a runoff with Assemblywoman Amy Demboski.

In the context of a debate on October 13, 2014, with co-host Bernadette Wilson over same-sex marriage, Berkowitz had said, "I support the idea of adults being able to choose who they have a relationship with.

Father and son should be allowed to marry, if they’re both consenting adults—if you’re defining marriage as the bundle of rights and privileges that’s now accrued to people, then yes.

In his inauguration speech he urged city residents and leaders to work to overcome differences and "rise above the immediacy and smallness of the moment".