BLM won the new contract after a pitch against a number of COI roster agencies.
It will work closely with creative agencies to develop the most effective communications strategies to reach Welsh audiences.
Marketing activity will be managed on a project-by-project basis. It is likely to include traditional marketing such as advertising and direct marketing, as well as digital marketing.
The Welsh Assembly spent £500,000 on media last year, according to Nielsen Media Research.
BLM media strategist Martin Greenbank said the agency won the account on the strength of its regional and digital credentials.
"COI recently handled a communications planning re-pitch for the Welsh Assembly," a COI spokesman said. "BLM has been appointed as a result."
Last year the Welsh Development Agency and Welsh Tourist Board were assimilated into the Welsh Assembly, which subsequently set up a new unit called the Department for Enterprise, Innovation and Networks. The latter's marketing division is led by former Welsh Tourist Board marketing head, Roger Pride.