diff --git a/client-api/src/api-types.ts b/client-api/src/api-types.ts
index e22000febf0a..07544c435106 100644
--- a/client-api/src/api-types.ts
+++ b/client-api/src/api-types.ts
@@ -26,7 +26,7 @@ export type DatasetStorageDetails = components["schemas"]["DatasetStorageDetails
 export type DatasetCollectionAttributes = components["schemas"]["DatasetCollectionAttributesResult"];
 export type ConcreteObjectStoreModel = components["schemas"]["ConcreteObjectStoreModel"];
 export type MessageException = components["schemas"]["MessageExceptionModel"];
-export type DatasetHash = components["schemas"]["DatasetHash-Output"];
+export type DatasetHash = components["schemas"]["DatasetHash"];
 export type DatasetSource = components["schemas"]["DatasetSource"];
 export type DatasetTransform = components["schemas"]["DatasetSourceTransform"];
 export type StoreExportPayload = components["schemas"]["StoreExportPayload"];
diff --git a/client/src/api/index.ts b/client/src/api/index.ts
index 3bf519095574..4f2ea81c5682 100644
--- a/client/src/api/index.ts
+++ b/client/src/api/index.ts
@@ -308,7 +308,7 @@ export function canMutateHistory(history: AnyHistory): boolean {
     return !history.purged && !history.archived;
 }
 
-export type DatasetHash = components["schemas"]["DatasetHash-Output"];
+export type DatasetHash = components["schemas"]["DatasetHash"];
 
 export type DatasetSource = components["schemas"]["DatasetSource"];
 export type DatasetTransform = components["schemas"]["DatasetSourceTransform"];
diff --git a/client/src/api/schema/schema.ts b/client/src/api/schema/schema.ts
index 29800bfa8dcc..09c4d57b37e6 100644
--- a/client/src/api/schema/schema.ts
+++ b/client/src/api/schema/schema.ts
@@ -7659,7 +7659,7 @@ export interface components {
             /** Ext */
             ext: string;
             /** Hashes */
-            hashes?: components["schemas"]["DatasetHash-Input"][] | null;
+            hashes?: components["schemas"]["FileHash"][] | null;
             /**
              * Identifier
              * @description A unique identifier for this element within the collection.
@@ -10101,17 +10101,7 @@ export interface components {
          */
         DatasetExtraFiles: components["schemas"]["ExtraFileEntry"][];
         /** DatasetHash */
-        "DatasetHash-Input": {
-            /**
-             * Hash Function
-             * @enum {string}
-             */
-            hash_function: "MD5" | "SHA-1" | "SHA-256" | "SHA-512";
-            /** Hash Value */
-            hash_value: string;
-        };
-        /** DatasetHash */
-        "DatasetHash-Output": {
+        DatasetHash: {
             /**
              * Extra Files Path
              * @description The path to the extra files used to generate the hash.
@@ -11730,6 +11720,16 @@ export interface components {
              */
             action_type: "fill_defaults";
         };
+        /** FileHash */
+        FileHash: {
+            /**
+             * Hash Function
+             * @enum {string}
+             */
+            hash_function: "MD5" | "SHA-1" | "SHA-256" | "SHA-512";
+            /** Hash Value */
+            hash_value: string;
+        };
         /** FileLibraryFolderItem */
         FileLibraryFolderItem: {
             /** Can Manage */
@@ -11855,7 +11855,7 @@ export interface components {
             /** Ext */
             ext: string;
             /** Hashes */
-            hashes?: components["schemas"]["DatasetHash-Input"][] | null;
+            hashes?: components["schemas"]["FileHash"][] | null;
             /** Info */
             info?: string | null;
             /** Location */
@@ -12725,7 +12725,7 @@ export interface components {
              * Hashes
              * @description The list of hashes associated with this dataset.
              */
-            hashes?: components["schemas"]["DatasetHash-Output"][] | null;
+            hashes?: components["schemas"]["DatasetHash"][] | null;
             /**
              * HDA or LDDA
              * @description Whether this dataset belongs to a history (HDA) or a library (LDDA).
@@ -12999,7 +12999,7 @@ export interface components {
              * Hashes
              * @description The list of hashes associated with this dataset.
              */
-            hashes: components["schemas"]["DatasetHash-Output"][];
+            hashes: components["schemas"]["DatasetHash"][];
             /**
              * HDA or LDDA
              * @description Whether this dataset belongs to a history (HDA) or a library (LDDA).
diff --git a/lib/galaxy/dependencies/pinned-requirements.txt b/lib/galaxy/dependencies/pinned-requirements.txt
index 340ff4c51761..e5a3ff3a1558 100644
--- a/lib/galaxy/dependencies/pinned-requirements.txt
+++ b/lib/galaxy/dependencies/pinned-requirements.txt
@@ -11,6 +11,7 @@ aiosignal==1.4.0
 alembic==1.16.5 ; python_full_version < '3.10'
 alembic==1.17.2 ; python_full_version >= '3.10'
 amqp==5.3.1
+annotated-doc==0.0.4
 annotated-types==0.7.0
 anyio==4.12.0
 apispec==6.8.4
@@ -70,7 +71,7 @@ edam-ontology==1.25.3
 email-validator==2.3.0
 et-xmlfile==2.0.0
 exceptiongroup==1.3.1
-fastapi==0.118.3
+fastapi==0.124.0
 filelock==3.19.1 ; python_full_version < '3.10'
 filelock==3.20.0 ; python_full_version >= '3.10'
 fissix==24.4.24
@@ -213,7 +214,8 @@ sortedcontainers==2.4.0
 spython==0.3.14
 sqlalchemy==2.0.44
 sqlparse==0.5.4
-starlette==0.48.0
+starlette==0.49.3 ; python_full_version < '3.10'
+starlette==0.50.0 ; python_full_version >= '3.10'
 starlette-context==0.4.0
 supervisor==4.3.0
 svgwrite==1.4.3
diff --git a/lib/galaxy/tool_util_models/parameters.py b/lib/galaxy/tool_util_models/parameters.py
index 135e5806291f..9d20e3cdbf7c 100644
--- a/lib/galaxy/tool_util_models/parameters.py
+++ b/lib/galaxy/tool_util_models/parameters.py
@@ -402,7 +402,7 @@ class DataRequestHdca(LegacyRequestModelAttributes):
     id: StrictStr
 
 
-class DatasetHash(StrictModel):
+class FileHash(StrictModel):
     hash_function: Literal["MD5", "SHA-1", "SHA-256", "SHA-512"]
     hash_value: StrictStr
 
@@ -416,7 +416,7 @@ class BaseDataRequest(StrictModel):
     created_from_basename: Optional[StrictStr] = None
     info: Optional[StrictStr] = None
     tags: Optional[List[str]] = None
-    hashes: Optional[List[DatasetHash]] = None
+    hashes: Optional[List[FileHash]] = None
     space_to_tab: bool = False
     to_posix_lines: bool = False
 
diff --git a/lib/galaxy/util/config_templates.py b/lib/galaxy/util/config_templates.py
index 996dcf818e76..b0b35e2df8a3 100644
--- a/lib/galaxy/util/config_templates.py
+++ b/lib/galaxy/util/config_templates.py
@@ -641,8 +641,6 @@ def _make_field_optional(field_info: FieldInfo):
     """Returns the field's definition to be used in a `create_model()` call to make the field optional."""
     annotation = field_info.annotation
     assert annotation is not None
-    if isinstance(annotation, type) and issubclass(annotation, BaseModel):
-        annotation = make_model_with_all_fields_optional(annotation)
     if field_info.is_required():
         return Annotated[Union[annotation, None], field_info], None
     else:
diff --git a/lib/galaxy/webapps/galaxy/api/users.py b/lib/galaxy/webapps/galaxy/api/users.py
index 7c89dd51ca2c..0cd485d81209 100644
--- a/lib/galaxy/webapps/galaxy/api/users.py
+++ b/lib/galaxy/webapps/galaxy/api/users.py
@@ -10,7 +10,6 @@
     Annotated,
     Any,
     Optional,
-    TYPE_CHECKING,
     Union,
 )
 
@@ -92,9 +91,7 @@
 )
 from galaxy.webapps.galaxy.api.common import UserIdPathParam
 from galaxy.webapps.galaxy.services.users import UsersService
-
-if TYPE_CHECKING:
-    from galaxy.work.context import SessionRequestContext
+from galaxy.work.context import SessionRequestContext
 
 log = logging.getLogger(__name__)
 
@@ -171,7 +168,7 @@ class FastAPIUsers:
     )
     def recalculate_disk_usage(
         self,
-        trans: "SessionRequestContext" = DependsOnTrans,
+        trans: SessionRequestContext = DependsOnTrans,
     ):
         """This route will be removed in a future version.
 
@@ -193,7 +190,7 @@ def recalculate_disk_usage(
     def recalculate_disk_usage_by_user_id(
         self,
         user_id: UserIdPathParam,
-        trans: "SessionRequestContext" = DependsOnTrans,
+        trans: SessionRequestContext = DependsOnTrans,
     ):
         result = self.service.recalculate_disk_usage(trans, user_id)
         return Response(status_code=status.HTTP_204_NO_CONTENT) if result is None else result
diff --git a/lib/galaxy/webapps/openapi/_compat/__init__.py b/lib/galaxy/webapps/openapi/_compat/__init__.py
new file mode 100644
index 000000000000..0b03aebab7e8
--- /dev/null
+++ b/lib/galaxy/webapps/openapi/_compat/__init__.py
@@ -0,0 +1,5 @@
+from .main import get_definitions as get_definitions
+
+__all__ = [
+    "get_definitions",
+]
diff --git a/lib/galaxy/webapps/openapi/_compat/main.py b/lib/galaxy/webapps/openapi/_compat/main.py
new file mode 100644
index 000000000000..1991a9137422
--- /dev/null
+++ b/lib/galaxy/webapps/openapi/_compat/main.py
@@ -0,0 +1,62 @@
+import sys
+from typing import (
+    Any,
+    Union,
+)
+
+from fastapi._compat import (
+    may_v1,
+    v2,
+)
+from fastapi._compat.model_field import ModelField
+from fastapi._compat.shared import PYDANTIC_V2
+from fastapi.types import ModelNameMap
+from typing_extensions import Literal
+
+from .v2 import (
+    GenerateJsonSchema as GenerateJsonSchema,
+    get_definitions as v2_get_definitions,
+)
+
+
+def get_definitions(
+    *,
+    fields: list[ModelField],
+    model_name_map: ModelNameMap,
+    separate_input_output_schemas: bool = True,
+    schema_generator: Union[GenerateJsonSchema, None] = None,
+) -> tuple[
+    dict[tuple[ModelField, Literal["validation", "serialization"]], may_v1.JsonSchemaValue],
+    dict[str, dict[str, Any]],
+]:
+    if sys.version_info < (3, 14):
+        v1_fields = [field for field in fields if isinstance(field, may_v1.ModelField)]
+        v1_field_maps, v1_definitions = may_v1.get_definitions(
+            fields=v1_fields,
+            model_name_map=model_name_map,
+            separate_input_output_schemas=separate_input_output_schemas,
+        )
+        if not PYDANTIC_V2:
+            return v1_field_maps, v1_definitions
+        else:
+            v2_fields = [field for field in fields if isinstance(field, v2.ModelField)]
+            v2_field_maps, v2_definitions = v2_get_definitions(
+                fields=v2_fields,
+                model_name_map=model_name_map,
+                separate_input_output_schemas=separate_input_output_schemas,
+                schema_generator=schema_generator,
+            )
+            all_definitions = {**v1_definitions, **v2_definitions}
+            all_field_maps = {**v1_field_maps, **v2_field_maps}
+            return all_field_maps, all_definitions
+
+    # Pydantic v1 is not supported since Python 3.14
+    else:
+        v2_fields = [field for field in fields if isinstance(field, v2.ModelField)]
+        v2_field_maps, v2_definitions = v2_get_definitions(
+            fields=v2_fields,
+            model_name_map=model_name_map,
+            separate_input_output_schemas=separate_input_output_schemas,
+            schema_generator=schema_generator,
+        )
+        return v2_field_maps, v2_definitions
diff --git a/lib/galaxy/webapps/openapi/_compat/v2.py b/lib/galaxy/webapps/openapi/_compat/v2.py
new file mode 100644
index 000000000000..ad6c5ea57ca0
--- /dev/null
+++ b/lib/galaxy/webapps/openapi/_compat/v2.py
@@ -0,0 +1,76 @@
+from collections.abc import Sequence
+from typing import (
+    Any,
+    cast,
+    Union,
+)
+
+from fastapi._compat.v2 import (
+    _has_computed_fields,
+    _remap_definitions_and_field_mappings,
+    get_flat_models_from_fields,
+    ModelField,
+)
+from fastapi.openapi.constants import REF_TEMPLATE
+from fastapi.types import ModelNameMap
+from pydantic.fields import FieldInfo as FieldInfo
+from pydantic.json_schema import (
+    GenerateJsonSchema as GenerateJsonSchema,
+    JsonSchemaValue as JsonSchemaValue,
+)
+from typing_extensions import Literal
+
+
+def get_definitions(
+    *,
+    fields: Sequence[ModelField],
+    model_name_map: ModelNameMap,
+    separate_input_output_schemas: bool = True,
+    schema_generator: Union[GenerateJsonSchema, None] = None,
+) -> tuple[
+    dict[tuple[ModelField, Literal["validation", "serialization"]], JsonSchemaValue],
+    dict[str, dict[str, Any]],
+]:
+    schema_generator = schema_generator or GenerateJsonSchema(ref_template=REF_TEMPLATE)
+    validation_fields = [field for field in fields if field.mode == "validation"]
+    serialization_fields = [field for field in fields if field.mode == "serialization"]
+    flat_validation_models = get_flat_models_from_fields(validation_fields, known_models=set())
+    flat_serialization_models = get_flat_models_from_fields(serialization_fields, known_models=set())
+    flat_validation_model_fields = [
+        ModelField(
+            field_info=FieldInfo(annotation=model),
+            name=model.__name__,
+            mode="validation",
+        )
+        for model in flat_validation_models
+    ]
+    flat_serialization_model_fields = [
+        ModelField(
+            field_info=FieldInfo(annotation=model),
+            name=model.__name__,
+            mode="serialization",
+        )
+        for model in flat_serialization_models
+    ]
+    flat_model_fields = flat_validation_model_fields + flat_serialization_model_fields
+    input_types = {f.type_ for f in fields}
+    unique_flat_model_fields = {f for f in flat_model_fields if f.type_ not in input_types}
+    inputs = [
+        (
+            field,
+            (field.mode if (separate_input_output_schemas or _has_computed_fields(field)) else "validation"),
+            field._type_adapter.core_schema,
+        )
+        for field in list(fields) + list(unique_flat_model_fields)
+    ]
+    field_mapping, definitions = schema_generator.generate_definitions(inputs=inputs)
+    for item_def in cast(dict[str, dict[str, Any]], definitions).values():
+        if "description" in item_def:
+            item_description = cast(str, item_def["description"]).split("\f")[0]
+            item_def["description"] = item_description
+    new_mapping, new_definitions = _remap_definitions_and_field_mappings(
+        model_name_map=model_name_map,
+        definitions=definitions,  # type: ignore[arg-type]
+        field_mapping=field_mapping,
+    )
+    return new_mapping, new_definitions
diff --git a/lib/galaxy/webapps/openapi/utils.py b/lib/galaxy/webapps/openapi/utils.py
index aef58fb97b5e..e0128b208776 100644
--- a/lib/galaxy/webapps/openapi/utils.py
+++ b/lib/galaxy/webapps/openapi/utils.py
@@ -1,5 +1,5 @@
 """
-Copy of https://github.com/tiangolo/fastapi/blob/master/fastapi/openapi/utils.py with changes from https://github.com/tiangolo/fastapi/pull/10903
+Copy of fastapi/openapi/utils.py from https://github.com/fastapi/fastapi/pull/13918
 """
 
 from collections.abc import Sequence
@@ -12,10 +12,8 @@
 from fastapi import routing
 from fastapi._compat import (
     get_compat_model_name_map,
-    get_definitions,
 )
 from fastapi.encoders import jsonable_encoder
-from fastapi.openapi.constants import REF_TEMPLATE
 from fastapi.openapi.models import OpenAPI
 from fastapi.openapi.utils import (
     get_fields_from_routes,
@@ -24,6 +22,8 @@
 from pydantic.json_schema import GenerateJsonSchema
 from starlette.routing import BaseRoute
 
+from ._compat import get_definitions
+
 
 def get_openapi(
     *,
@@ -40,6 +40,7 @@ def get_openapi(
     contact: Optional[dict[str, Union[str, Any]]] = None,
     license_info: Optional[dict[str, Union[str, Any]]] = None,
     separate_input_output_schemas: bool = True,
+    external_docs: Optional[dict[str, Any]] = None,
     schema_generator: Optional[GenerateJsonSchema] = None,
 ) -> dict[str, Any]:
     info: dict[str, Any] = {"title": title, "version": version}
@@ -62,19 +63,17 @@ def get_openapi(
     operation_ids: set[str] = set()
     all_fields = get_fields_from_routes(list(routes or []) + list(webhooks or []))
     model_name_map = get_compat_model_name_map(all_fields)
-    schema_generator = schema_generator or GenerateJsonSchema(ref_template=REF_TEMPLATE)
     field_mapping, definitions = get_definitions(
         fields=all_fields,
-        schema_generator=schema_generator,
         model_name_map=model_name_map,
         separate_input_output_schemas=separate_input_output_schemas,
+        schema_generator=schema_generator,
     )
     for route in routes or []:
         if isinstance(route, routing.APIRoute):
             result = get_openapi_path(
                 route=route,
                 operation_ids=operation_ids,
-                schema_generator=schema_generator,
                 model_name_map=model_name_map,
                 field_mapping=field_mapping,
                 separate_input_output_schemas=separate_input_output_schemas,
@@ -92,7 +91,6 @@ def get_openapi(
             result = get_openapi_path(
                 route=webhook,
                 operation_ids=operation_ids,
-                schema_generator=schema_generator,
                 model_name_map=model_name_map,
                 field_mapping=field_mapping,
                 separate_input_output_schemas=separate_input_output_schemas,
@@ -114,4 +112,6 @@ def get_openapi(
         output["webhooks"] = webhook_paths
     if tags:
         output["tags"] = tags
+    if external_docs:
+        output["externalDocs"] = external_docs
     return jsonable_encoder(OpenAPI(**output), by_alias=True, exclude_none=True)
diff --git a/packages/tool_shed/setup.cfg b/packages/tool_shed/setup.cfg
index 87a1dfee1777..99f0069ac05e 100644
--- a/packages/tool_shed/setup.cfg
+++ b/packages/tool_shed/setup.cfg
@@ -42,7 +42,7 @@ install_requires =
     galaxy-web-apps
     a2wsgi
     alembic
-    fastapi>=0.111.0,!=0.119.*,!=0.120.*,!=0.121.*,!=0.122.*,!=0.123.0
+    fastapi>=0.124.0
     Mako
     MarkupSafe
     mercurial>=6.8.2
diff --git a/packages/web_apps/setup.cfg b/packages/web_apps/setup.cfg
index d5602c98e8ec..9c5605e7e5e3 100644
--- a/packages/web_apps/setup.cfg
+++ b/packages/web_apps/setup.cfg
@@ -43,7 +43,7 @@ install_requires =
     apispec
     Babel
     CT3>=3.3.3
-    fastapi>=0.111.0,!=0.119.*,!=0.120.*,!=0.121.*,!=0.122.*,!=0.123.0
+    fastapi>=0.124.0
     gunicorn
     httpx
     gxformat2
diff --git a/pyproject.toml b/pyproject.toml
index b67c4eebcf9d..ebf1812eb939 100644
--- a/pyproject.toml
+++ b/pyproject.toml
@@ -37,7 +37,7 @@ dependencies = [
     "docutils!=0.17,!=0.17.1",
     "dparse",
     "edam-ontology",
-    "fastapi>=0.111.0,!=0.119.*,!=0.120.*,!=0.121.*,!=0.122.*,!=0.123.0",  # https://github.com/fastapi/fastapi/pull/13918
+    "fastapi>=0.124.0",  # https://github.com/fastapi/fastapi/pull/14453
     "fissix",
     "fs",
     "future>=1.0.0",  # Python 3.12 support