diff --git a/lib/galaxy/managers/genomes.py b/lib/galaxy/managers/genomes.py
index f6af2d73d9a7..74ccdc521933 100644
--- a/lib/galaxy/managers/genomes.py
+++ b/lib/galaxy/managers/genomes.py
@@ -4,7 +4,10 @@
     TYPE_CHECKING,
 )
 
-from sqlalchemy import func
+from sqlalchemy import (
+    func,
+    text,
+)
 
 from galaxy import model as m
 from galaxy.exceptions import (
@@ -75,6 +78,7 @@ def _get_index_filename(self, id, tbl_entries, ext, index_type):
 
 class GenomeFilterMixin:
     orm_filter_parsers: "OrmFilterParsersType"
+    database_connection: str
     valid_ops = ("eq", "contains", "has")
 
     def create_genome_filter(self, attr, op, val):
@@ -86,15 +90,21 @@ def _create_genome_filter(model_class=None):
             # Doesn't filter genome_build for collections
             if model_class.__name__ == "HistoryDatasetCollectionAssociation":
                 return False
-            column = func.json_extract(model_class.table.c._metadata, "$.dbkey")
+            # TODO: should use is_postgres(self.database_connection) in 23.2
+            if self.database_connection.startswith("postgres"):
+                column = text("convert_from(metadata, 'UTF8')::json ->> 'dbkey'")
+            else:
+                column = func.json_extract(model_class.table.c._metadata, "$.dbkey")
             lower_val = val.lower()  # Ignore case
+            # dbkey can either be "hg38" or '["hg38"]', so we need to check both
             if op == "eq":
-                cond = func.lower(column) == lower_val
+                cond = func.lower(column) == lower_val or func.lower(column) == f'["{lower_val}"]'
             else:
                 cond = func.lower(column).contains(lower_val, autoescape=True)
             return cond
 
         return _create_genome_filter
 
-    def _add_parsers(self):
+    def _add_parsers(self, database_connection: str):
+        self.database_connection = database_connection
         self.orm_filter_parsers.update({"genome_build": self.create_genome_filter})
diff --git a/lib/galaxy/managers/history_contents.py b/lib/galaxy/managers/history_contents.py
index 6acd74bf5a07..6767ebbbfc39 100644
--- a/lib/galaxy/managers/history_contents.py
+++ b/lib/galaxy/managers/history_contents.py
@@ -632,8 +632,9 @@ def parse_type_id_list(self, type_id_list_string, sep=","):
 
     def _add_parsers(self):
         super()._add_parsers()
+        database_connection: str = self.app.config.database_connection
         annotatable.AnnotatableFilterMixin._add_parsers(self)
-        genomes.GenomeFilterMixin._add_parsers(self)
+        genomes.GenomeFilterMixin._add_parsers(self, database_connection)
         deletable.PurgableFiltersMixin._add_parsers(self)
         taggable.TaggableFilterMixin._add_parsers(self)
         tools.ToolFilterMixin._add_parsers(self)