diff --git a/lib/tool_shed/managers/repositories.py b/lib/tool_shed/managers/repositories.py
index 58f2158c5cd3..e7af6ff641bf 100644
--- a/lib/tool_shed/managers/repositories.py
+++ b/lib/tool_shed/managers/repositories.py
@@ -273,8 +273,7 @@ def get_repository_metadata_for_management(
     trans: ProvidesUserContext, encoded_repository_id: str, changeset_revision: str
 ) -> RepositoryMetadata:
     repository = get_repository_in_tool_shed(trans.app, encoded_repository_id)
-    if not can_manage_repo(trans, repository):
-        raise InsufficientPermissionsException("Cannot manage target repository")
+    ensure_can_manage(trans, repository, "Cannot manage target repository")
     revisions = [r for r in repository.metadata_revisions if r.changeset_revision == changeset_revision]
     if len(revisions) != 1:
         raise ObjectNotFound()
@@ -582,6 +581,12 @@ def upload_tar_and_set_metadata(
     return message
 
 
+def ensure_can_manage(trans: ProvidesUserContext, repository: Repository, error_message: Optional[str] = None) -> None:
+    if not can_manage_repo(trans, repository):
+        error_message = error_message or "You do not have permission to update this repository."
+        raise InsufficientPermissionsException(error_message)
+
+
 def _get_repository_by_name_and_owner(session: scoped_session, name: str, owner: str, user_model):
     stmt = (
         select(Repository)
diff --git a/lib/tool_shed/test/base/populators.py b/lib/tool_shed/test/base/populators.py
index 01cc8eea6937..642c1b76b9ac 100644
--- a/lib/tool_shed/test/base/populators.py
+++ b/lib/tool_shed/test/base/populators.py
@@ -23,6 +23,7 @@
     Category,
     CreateCategoryRequest,
     CreateRepositoryRequest,
+    DetailedRepository,
     from_legacy_install_info,
     GetInstallInfoRequest,
     GetOrderedInstallableRevisionsRequest,
@@ -41,6 +42,7 @@
     ResetMetadataOnRepositoryResponse,
     ToolSearchRequest,
     ToolSearchResults,
+    UpdateRepositoryRequest,
     Version,
 )
 from .api_util import (
@@ -209,6 +211,17 @@ def upload_revision_raw(
         )
         return response
 
+    def update_raw(self, repository: HasRepositoryId, request: UpdateRepositoryRequest) -> requests.Response:
+        repository_id = self._repository_id(repository)
+        body_json = request.model_dump(exclude_unset=True, by_alias=True)
+        put_response = self._api_interactor.put(f"repositories/{repository_id}", json=body_json)
+        return put_response
+
+    def update(self, repository: HasRepositoryId, request: UpdateRepositoryRequest) -> Repository:
+        response = self.update_raw(repository, request)
+        api_asserts.assert_status_code_is_ok(response)
+        return Repository(**response.json())
+
     def upload_revision(
         self, repository: HasRepositoryId, path: Traversable, commit_message: str = DEFAULT_COMMIT_MESSAGE
     ) -> RepositoryUpdate:
@@ -358,11 +371,14 @@ def unset_deprecated(self, repository: HasRepositoryId):
         delete_response = self._api_interactor.delete(f"repositories/{repository_id}/deprecated")
         delete_response.raise_for_status()
 
-    def is_deprecated(self, repository: HasRepositoryId) -> bool:
+    def get_repository(self, repository: HasRepositoryId) -> DetailedRepository:
         repository_id = self._repository_id(repository)
         repository_response = self._api_interactor.get(f"repositories/{repository_id}")
         repository_response.raise_for_status()
-        return Repository(**repository_response.json()).deprecated
+        return DetailedRepository(**repository_response.json())
+
+    def is_deprecated(self, repository: HasRepositoryId) -> bool:
+        return self.get_repository(repository).deprecated
 
     def get_metadata(self, repository: HasRepositoryId, downloadable_only=True) -> RepositoryMetadata:
         repository_id = self._repository_id(repository)
diff --git a/lib/tool_shed/test/functional/test_shed_repositories.py b/lib/tool_shed/test/functional/test_shed_repositories.py
index fe7c4d3bac24..2ab544bf438e 100644
--- a/lib/tool_shed/test/functional/test_shed_repositories.py
+++ b/lib/tool_shed/test/functional/test_shed_repositories.py
@@ -10,7 +10,10 @@
     HasRepositoryId,
     repo_tars,
 )
-from tool_shed_client.schema import RepositoryRevisionMetadata
+from tool_shed_client.schema import (
+    RepositoryRevisionMetadata,
+    UpdateRepositoryRequest,
+)
 from ..base.api import (
     ShedApiTestCase,
     skip_if_api_v1,
@@ -49,6 +52,40 @@ def test_update_repository(self):
         )
         assert repository_update.is_ok
 
+    def test_update_repository_info(self):
+        populator = self.populator
+        prefix = "testupdateinfo"
+        category_id = populator.new_category(prefix=prefix).id
+        repository = populator.new_repository(category_id, prefix=prefix)
+        repository_id = repository.id
+        request = UpdateRepositoryRequest(homepage_url="https://www.google.com")
+        update = populator.update(repository_id, request)
+        assert update.homepage_url == "https://www.google.com"
+        assert populator.get_repository(repository_id).homepage_url == "https://www.google.com"
+
+    def test_update_category(self):
+        populator = self.populator
+        prefix = "testupdatecategory"
+
+        old_category_id = populator.new_category(prefix=prefix).id
+        new_category_id = populator.new_category(prefix=prefix).id
+
+        populator.assert_category_has_n_repositories(old_category_id, 0)
+        populator.assert_category_has_n_repositories(new_category_id, 0)
+
+        repository = populator.new_repository(old_category_id, prefix=prefix)
+        repository_id = repository.id
+
+        populator.assert_category_has_n_repositories(old_category_id, 1)
+        populator.assert_category_has_n_repositories(new_category_id, 0)
+
+        request = UpdateRepositoryRequest(category_ids=[new_category_id])
+        update = populator.update(repository_id, request)
+
+        # does this mean we cannot remove categories?
+        populator.assert_category_has_n_repositories(old_category_id, 0)
+        populator.assert_category_has_n_repositories(new_category_id, 1)
+
     # used by getRepository in TS client.
     def test_metadata_simple(self):
         populator = self.populator
diff --git a/lib/tool_shed/util/repository_util.py b/lib/tool_shed/util/repository_util.py
index 32829078f661..51c9ae6d1155 100644
--- a/lib/tool_shed/util/repository_util.py
+++ b/lib/tool_shed/util/repository_util.py
@@ -432,17 +432,27 @@ def change_repository_name_in_hgrc_file(hgrc_file: str, new_name: str) -> None:
 def update_repository(trans: "ProvidesUserContext", id: str, **kwds) -> Tuple[Optional["Repository"], Optional[str]]:
     """Update an existing ToolShed repository"""
     app = trans.app
-    message = None
-    flush_needed = False
     sa_session = app.model.session
     repository = sa_session.get(app.model.Repository, app.security.decode_id(id))
     if repository is None:
         return None, "Unknown repository ID"
 
-    if not (trans.user_is_admin or trans.app.security_agent.user_can_administer_repository(trans.user, repository)):
+    if not (trans.user_is_admin or app.security_agent.user_can_administer_repository(trans.user, repository)):
         message = "You are not the owner of this repository, so you cannot administer it."
         return None, message
 
+    return update_validated_repository(trans, repository, **kwds)
+
+
+def update_validated_repository(
+    trans: "ProvidesUserContext", repository: "Repository", **kwds
+) -> Tuple[Optional["Repository"], Optional[str]]:
+    """Update an existing ToolShed repository metadata once permissions have been checked."""
+    app = trans.app
+    sa_session = app.model.session
+    message = None
+    flush_needed = False
+
     # Allowlist properties that can be changed via this method
     for key in ("type", "description", "long_description", "remote_repository_url", "homepage_url"):
         # If that key is available, not None and different than what's in the model
@@ -451,10 +461,9 @@ def update_repository(trans: "ProvidesUserContext", id: str, **kwds) -> Tuple[Op
             flush_needed = True
 
     if "category_ids" in kwds and isinstance(kwds["category_ids"], list):
+
         # Remove existing category associations
-        delete_repository_category_associations(
-            sa_session, app.model.RepositoryCategoryAssociation, app.security.decode_id(id)
-        )
+        delete_repository_category_associations(sa_session, app.model.RepositoryCategoryAssociation, repository.id)
 
         # Then (re)create category associations
         for category_id in kwds["category_ids"]:
diff --git a/lib/tool_shed/webapp/api2/repositories.py b/lib/tool_shed/webapp/api2/repositories.py
index ef510c088888..b20f3fc020d3 100644
--- a/lib/tool_shed/webapp/api2/repositories.py
+++ b/lib/tool_shed/webapp/api2/repositories.py
@@ -19,7 +19,10 @@
 )
 from starlette.datastructures import UploadFile as StarletteUploadFile
 
-from galaxy.exceptions import InsufficientPermissionsException
+from galaxy.exceptions import (
+    ActionInputError,
+    InsufficientPermissionsException,
+)
 from galaxy.model.base import transaction
 from galaxy.webapps.galaxy.api import as_form
 from tool_shed.context import SessionRequestContext
@@ -28,6 +31,7 @@
     can_update_repo,
     check_updates,
     create_repository,
+    ensure_can_manage,
     get_install_info,
     get_ordered_installable_revisions,
     get_repository_metadata_dict,
@@ -42,7 +46,10 @@
     upload_tar_and_set_metadata,
 )
 from tool_shed.structured_app import ToolShedApp
-from tool_shed.util.repository_util import get_repository_in_tool_shed
+from tool_shed.util.repository_util import (
+    get_repository_in_tool_shed,
+    update_validated_repository,
+)
 from tool_shed_client.schema import (
     CreateRepositoryRequest,
     DetailedRepository,
@@ -57,6 +64,7 @@
     RepositoryUpdateRequest,
     ResetMetadataOnRepositoryRequest,
     ResetMetadataOnRepositoryResponse,
+    UpdateRepositoryRequest,
     ValidRepostiroyUpdateMessage,
 )
 from . import (
@@ -293,6 +301,28 @@ def show(
         repository = get_repository_in_tool_shed(self.app, encoded_repository_id)
         return to_detailed_model(self.app, repository)
 
+    @router.put(
+        "/api/repositories/{encoded_repository_id}",
+        operation_id="repositories__update_repository",
+    )
+    def update_repository(
+        self,
+        trans: SessionRequestContext = DependsOnTrans,
+        encoded_repository_id: str = RepositoryIdPathParam,
+        request: UpdateRepositoryRequest = Body(...),
+    ) -> DetailedRepository:
+        repository = get_repository_in_tool_shed(self.app, encoded_repository_id)
+        ensure_can_manage(trans, repository)
+
+        # may want to set some of these to null, so we're using the exclude_unset feature
+        # to just serialize the ones we want to use to a dictionary.
+        update_dictionary = request.model_dump(exclude_unset=True)
+        repo_result, message = update_validated_repository(trans, repository, **update_dictionary)
+        if repo_result is None:
+            raise ActionInputError(message)
+
+        return to_detailed_model(self.app, repository)
+
     @router.get(
         "/api/repositories/{encoded_repository_id}/permissions",
         operation_id="repositories__permissions",
@@ -323,8 +353,7 @@ def show_allow_push(
         encoded_repository_id: str = RepositoryIdPathParam,
     ) -> List[str]:
         repository = get_repository_in_tool_shed(self.app, encoded_repository_id)
-        if not can_manage_repo(trans, repository):
-            raise InsufficientPermissionsException("You do not have permission to update this repository.")
+        ensure_can_manage(trans, repository)
         return trans.app.security_agent.usernames_that_can_push(repository)
 
     @router.post(
@@ -390,8 +419,7 @@ def set_deprecated(
         encoded_repository_id: str = RepositoryIdPathParam,
     ):
         repository = get_repository_in_tool_shed(self.app, encoded_repository_id)
-        if not can_manage_repo(trans, repository):
-            raise InsufficientPermissionsException("You do not have permission to update this repository.")
+        ensure_can_manage(trans, repository)
         repository.deprecated = True
         trans.sa_session.add(repository)
         with transaction(trans.sa_session):
@@ -409,8 +437,7 @@ def unset_deprecated(
         encoded_repository_id: str = RepositoryIdPathParam,
     ):
         repository = get_repository_in_tool_shed(self.app, encoded_repository_id)
-        if not can_manage_repo(trans, repository):
-            raise InsufficientPermissionsException("You do not have permission to update this repository.")
+        ensure_can_manage(trans, repository)
         repository.deprecated = False
         trans.sa_session.add(repository)
         with transaction(trans.sa_session):
diff --git a/lib/tool_shed/webapp/frontend/src/schema/schema.ts b/lib/tool_shed/webapp/frontend/src/schema/schema.ts
index 8122e6ae0647..e01c0b0fe8c3 100644
--- a/lib/tool_shed/webapp/frontend/src/schema/schema.ts
+++ b/lib/tool_shed/webapp/frontend/src/schema/schema.ts
@@ -101,6 +101,8 @@ export interface paths {
     "/api/repositories/{encoded_repository_id}": {
         /** Show */
         get: operations["repositories__show"]
+        /** Update Repository */
+        put: operations["repositories__update_repository"]
     }
     "/api/repositories/{encoded_repository_id}/allow_push": {
         /** Show Allow Push */
@@ -2093,6 +2095,23 @@ export interface components {
             /** Email */
             email: string
         }
+        /** UpdateRepositoryRequest */
+        UpdateRepositoryRequest: {
+            /** Category IDs */
+            "category_ids[]"?: string[] | string | null
+            /** Description */
+            description?: string | null
+            /** Homepage Url */
+            homepage_url?: string | null
+            /** Name */
+            name?: string | null
+            /** Remote Repository Url */
+            remote_repository_url?: string | null
+            /** Synopsis */
+            synopsis?: string | null
+            /** Type */
+            type?: ("repository_suite_definition" | "tool_dependency_definition" | "unrestricted") | null
+        }
         /** UserV2 */
         UserV2: {
             /** Id */
@@ -2701,6 +2720,40 @@ export interface operations {
             }
         }
     }
+    /** Update Repository */
+    repositories__update_repository: {
+        parameters: {
+            path: {
+                /** @description The encoded database identifier of the repository. */
+                encoded_repository_id: string
+            }
+        }
+        requestBody: {
+            content: {
+                "application/json": components["schemas"]["UpdateRepositoryRequest"]
+            }
+        }
+        responses: {
+            /** @description Successful Response */
+            200: {
+                content: {
+                    "application/json": components["schemas"]["DetailedRepository"]
+                }
+            }
+            /** @description Request Error */
+            "4XX": {
+                content: {
+                    "application/json": components["schemas"]["MessageExceptionModel"]
+                }
+            }
+            /** @description Server Error */
+            "5XX": {
+                content: {
+                    "application/json": components["schemas"]["MessageExceptionModel"]
+                }
+            }
+        }
+    }
     /** Show Allow Push */
     repositories__show_allow_push: {
         parameters: {
diff --git a/lib/tool_shed_client/schema/__init__.py b/lib/tool_shed_client/schema/__init__.py
index 42c890ad4afd..ebf5a0a850a0 100644
--- a/lib/tool_shed_client/schema/__init__.py
+++ b/lib/tool_shed_client/schema/__init__.py
@@ -123,6 +123,25 @@ class CreateRepositoryRequest(BaseModel):
     model_config = ConfigDict(populate_by_name=True)
 
 
+class UpdateRepositoryRequest(BaseModel):
+    name: Optional[str] = None
+    synopsis: Optional[str] = None
+    type_: Optional[RepositoryType] = Field(
+        None,
+        alias="type",
+        title="Type",
+    )
+    description: Optional[str] = None
+    remote_repository_url: Optional[str] = None
+    homepage_url: Optional[str] = None
+    category_ids: Optional[List[str]] = Field(
+        None,
+        alias="category_ids",
+        title="Category IDs",
+    )
+    model_config = ConfigDict(populate_by_name=True)
+
+
 class RepositoryUpdateRequest(BaseModel):
     commit_message: Optional[str] = None