The map is made from genetic analyses of about 900 parts of three brains and contains more than 100 million gene expression measurements.
The team, from the Allen Institute for Brain Science in Seattle and Edinburgh University, said the project might help understand how genetic disorders cause brain disease.
The study appears in Nature journal.
The human brain is the most complex structure in the world, composed of 100 billion cells, but it is still not fully understood. Prof Ed Lein, from the Allen Institute for Brain Science, one of the authors of the paper, said this atlas could provide vital information in the general understanding of "brain function, development, evolution and disease".
The teams says that the majority of genes in the human brain are expressed in patterns very similar from one brain to another - showing that despite different individual personalities, our brains are in fact strikingly similar.
Although the human genome was sequenced some time ago, it was now "essential to understand how it makes all of the genes and where they are expressed in the human brain", said Prof Seth Grant from the neuroscience department at Edinburgh University.
Before mapping the human brain, the researchers had spent years performing similar studies on mice. But since in people the organ is a lot more complex, they had to modify their approach to get the best results.
After cutting individual brains into tiny pieces, the scientists analysed each piece using computer software to work out the pattern of gene expression in the brain. "In the earlier studies, individual genes were studied in the mouse brain, and each one was mapped one at a time to find where in the brain they are expressed," said Prof Grant.
"But now we took each little piece of brain tissue and measured all genes all at once using array technology."