The Stair Park have promoted from within following the departure of Stevie Farrell with Hamill, 34, being handed his first managerial role.
His backroom team will comprise two other Stranraer team-mates with Daryl Duffy being named assistant manager and Scott Robertson stepping up to become player-coach.
Since arriving at Stair Park, former Hearts, Kilmarnock and Queen of the South midfielder Hamill become increasingly involved on the coaching side.
Duffy, 37, who recently completed his UEFA B Licence, only joined Stranraer last summer but quickly became a key figure in the Blues promotion .
He began his career with Rangers and has since played for a host of clubs at home and abroad, including Falkirk, Hull City, Swansea City, Hibernian and Airdrie.
Robertson, 33, joined Stranraer in 2013 after spells with Stirling Albion, Partick Thistle and Arbroath. He left for Airdrie in 2018 but returned to Stair Park the following year and has now racked up over 250 appearances.
Chairman Shaun Niven said: "This is an exciting time for the club and a great opportunity for our new management team.
“I know they are keen to get started and I’m delighted that Jamie, Darryl and Scott have agreed to come on board.”
Duffy tweeted: "Absolutely buzzing! Been speaking to Hammy and Robbo more than my own family this week and long may it continue. Lots of work to get through in a short space of time. Let's go!"