diff --git a/client/src/api/schema/schema.ts b/client/src/api/schema/schema.ts
index 23baa4dc094e..0a748e04031c 100644
--- a/client/src/api/schema/schema.ts
+++ b/client/src/api/schema/schema.ts
@@ -3047,7 +3047,7 @@ export interface paths {
          * @deprecated
          * @description This endpoint is deprecated. Please use POST /api/folders/{folder_id} or POST /api/folders/{folder_id}/contents instead.
          */
-        post: operations["create_api_libraries__library_id__contents_post"];
+        post: operations["create_form_api_libraries__library_id__contents_post"];
         delete?: never;
         options?: never;
         head?: never;
@@ -6079,6 +6079,70 @@ export interface components {
             /** Name */
             name?: unknown;
         };
+        /** Body_create_form_api_libraries__library_id__contents_post */
+        Body_create_form_api_libraries__library_id__contents_post: {
+            /** Create Type */
+            create_type: unknown;
+            /**
+             * Dbkey
+             * @default ?
+             */
+            dbkey: unknown;
+            /** Extended Metadata */
+            extended_metadata?: unknown;
+            /** File Type */
+            file_type?: unknown;
+            /** Files */
+            files?: string[] | null;
+            /**
+             * Filesystem Paths
+             * @default
+             */
+            filesystem_paths: unknown;
+            /** Folder Id */
+            folder_id: unknown;
+            /** From Hda Id */
+            from_hda_id?: unknown;
+            /** From Hdca Id */
+            from_hdca_id?: unknown;
+            /**
+             * Ldda Message
+             * @default
+             */
+            ldda_message: unknown;
+            /**
+             * Link Data Only
+             * @default copy_files
+             */
+            link_data_only: unknown;
+            /**
+             * Roles
+             * @default
+             */
+            roles: unknown;
+            /**
+             * Server Dir
+             * @default
+             */
+            server_dir: unknown;
+            /**
+             * Tag Using Filenames
+             * @default false
+             */
+            tag_using_filenames: unknown;
+            /**
+             * Tags
+             * @default []
+             */
+            tags: unknown;
+            /**
+             * Upload Option
+             * @default upload_file
+             */
+            upload_option: unknown;
+            /** Uuid */
+            uuid?: unknown;
+        };
         /** Body_fetch_form_api_tools_fetch_post */
         Body_fetch_form_api_tools_fetch_post: {
             /** Files */
@@ -12876,7 +12940,7 @@ export interface components {
              * if True, copy the elements into the collection
              * @default false
              */
-            copy_elements: boolean | null;
+            copy_elements: boolean;
             /** the type of item to create */
             create_type: components["schemas"]["CreateType"];
             /** list of dictionaries containing the element identifiers for the collection */
@@ -12896,29 +12960,29 @@ export interface components {
              * if True, hide the source items in the collection
              * @default false
              */
-            hide_source_items: boolean | null;
+            hide_source_items: boolean;
             /**
              * the new message attribute of the LDDA created
              * @default
              */
-            ldda_message: string | null;
+            ldda_message: string;
             /** the name of the collection */
             name?: string | null;
             /**
              * create tags on datasets using the file's original name
              * @default false
              */
-            tag_using_filenames: boolean | null;
+            tag_using_filenames: boolean;
             /**
              * create the given list of tags on datasets
              * @default []
              */
-            tags: string[] | null;
+            tags: string[];
             /**
              * the method to use for uploading files
              * @default upload_file
              */
-            upload_option: components["schemas"]["UploadOption"] | null;
+            upload_option: components["schemas"]["UploadOption"];
         };
         /** LibraryContentsCreateDatasetCollectionResponse */
         LibraryContentsCreateDatasetCollectionResponse: components["schemas"]["LibraryContentsCreateDatasetResponse"][];
@@ -13004,7 +13068,7 @@ export interface components {
              * if True, purge the library dataset
              * @default false
              */
-            purge: boolean | null;
+            purge: boolean;
         };
         /** LibraryContentsDeleteResponse */
         LibraryContentsDeleteResponse: {
@@ -13024,7 +13088,7 @@ export interface components {
              * database key
              * @default ?
              */
-            dbkey: string | unknown[] | null;
+            dbkey: string | unknown[];
             /** sub-dictionary containing any extended metadata to associate with the item */
             extended_metadata?: Record<string, never> | null;
             /** file type */
@@ -13033,7 +13097,7 @@ export interface components {
              * (only if upload_option is 'upload_paths' and the user is an admin) file paths on the Galaxy server to upload to the library, one file per line
              * @default
              */
-            filesystem_paths: string | null;
+            filesystem_paths: string;
             /**
              * the encoded id of the parent folder of the new item
              * @example 0123456789ABCDEF
@@ -13047,39 +13111,41 @@ export interface components {
              * the new message attribute of the LDDA created
              * @default
              */
-            ldda_message: string | null;
+            ldda_message: string;
             /**
              * (only when upload_option is 'upload_directory' or 'upload_paths').Setting to 'link_to_files' symlinks instead of copying the files
              * @default copy_files
              */
-            link_data_only: components["schemas"]["LinkDataOnly"] | null;
+            link_data_only: components["schemas"]["LinkDataOnly"];
             /**
              * user selected roles
              * @default
              */
-            roles: string | null;
+            roles: string;
             /**
              * (only if upload_option is 'upload_directory') relative path of the subdirectory of Galaxy ``library_import_dir`` (if admin) or ``user_library_import_dir`` (if non-admin) to upload. All and only the files (i.e. no subdirectories) contained in the specified directory will be uploaded.
              * @default
              */
-            server_dir: string | null;
+            server_dir: string;
             /**
              * create tags on datasets using the file's original name
              * @default false
              */
-            tag_using_filenames: boolean | null;
+            tag_using_filenames: boolean;
             /**
              * create the given list of tags on datasets
              * @default []
              */
-            tags: string[] | null;
+            tags: string[];
             /**
              * the method to use for uploading files
              * @default upload_file
              */
-            upload_option: components["schemas"]["UploadOption"] | null;
+            upload_option: components["schemas"]["UploadOption"];
             /** UUID of the dataset to upload */
             uuid?: string | null;
+        } & {
+            [key: string]: unknown;
         };
         /** LibraryContentsFolderCreatePayload */
         LibraryContentsFolderCreatePayload: {
@@ -13089,7 +13155,7 @@ export interface components {
              * description of the folder to create
              * @default
              */
-            description: string | null;
+            description: string;
             /** sub-dictionary containing any extended metadata to associate with the item */
             extended_metadata?: Record<string, never> | null;
             /**
@@ -13105,27 +13171,27 @@ export interface components {
              * the new message attribute of the LDDA created
              * @default
              */
-            ldda_message: string | null;
+            ldda_message: string;
             /**
              * name of the folder to create
              * @default
              */
-            name: string | null;
+            name: string;
             /**
              * create tags on datasets using the file's original name
              * @default false
              */
-            tag_using_filenames: boolean | null;
+            tag_using_filenames: boolean;
             /**
              * create the given list of tags on datasets
              * @default []
              */
-            tags: string[] | null;
+            tags: string[];
             /**
              * the method to use for uploading files
              * @default upload_file
              */
-            upload_option: components["schemas"]["UploadOption"] | null;
+            upload_option: components["schemas"]["UploadOption"];
         };
         /** LibraryContentsIndexDatasetResponse */
         LibraryContentsIndexDatasetResponse: {
@@ -27929,7 +27995,7 @@ export interface operations {
             };
         };
     };
-    create_api_libraries__library_id__contents_post: {
+    create_form_api_libraries__library_id__contents_post: {
         parameters: {
             query?: never;
             header?: {
@@ -27943,10 +28009,7 @@ export interface operations {
         };
         requestBody: {
             content: {
-                "application/json":
-                    | components["schemas"]["LibraryContentsFolderCreatePayload"]
-                    | components["schemas"]["LibraryContentsFileCreatePayload"]
-                    | components["schemas"]["LibraryContentsCollectionCreatePayload"];
+                "multipart/form-data": components["schemas"]["Body_create_form_api_libraries__library_id__contents_post"];
             };
         };
         responses: {
diff --git a/lib/galaxy/actions/library.py b/lib/galaxy/actions/library.py
index a10098da9400..439953dfe467 100644
--- a/lib/galaxy/actions/library.py
+++ b/lib/galaxy/actions/library.py
@@ -125,6 +125,8 @@ def _upload_dataset(self, trans, folder_id: int, payload):
             raise exceptions.InvalidFileFormatError("Invalid folder specified")
         # Proceed with (mostly) regular upload processing if we're still errorless
         if payload.upload_option == "upload_file":
+            for i, upload_dataset in enumerate(tool_params["files"]):
+                upload_dataset["file_data"] = payload.files[i]
             tool_params = upload_common.persist_uploads(tool_params, trans)
             uploaded_datasets = upload_common.get_uploaded_datasets(
                 trans, cntrller, tool_params, dataset_upload_inputs, library_bunch=library_bunch
diff --git a/lib/galaxy/schema/library_contents.py b/lib/galaxy/schema/library_contents.py
index c692c062da26..44d3e8191619 100644
--- a/lib/galaxy/schema/library_contents.py
+++ b/lib/galaxy/schema/library_contents.py
@@ -1,3 +1,4 @@
+import json
 from enum import Enum
 from typing import (
     Any,
@@ -12,6 +13,7 @@
     Field,
     RootModel,
 )
+from pydantic.functional_validators import field_validator
 from typing_extensions import (
     Annotated,
     Literal,
@@ -52,7 +54,7 @@ class LibraryContentsCreatePayload(Model):
         ...,
         title="the type of item to create",
     )
-    upload_option: Optional[UploadOption] = Field(
+    upload_option: UploadOption = Field(
         UploadOption.upload_file,
         title="the method to use for uploading files",
     )
@@ -60,11 +62,11 @@ class LibraryContentsCreatePayload(Model):
         ...,
         title="the encoded id of the parent folder of the new item",
     )
-    tag_using_filenames: Optional[bool] = Field(
+    tag_using_filenames: bool = Field(
         False,
         title="create tags on datasets using the file's original name",
     )
-    tags: Optional[List[str]] = Field(
+    tags: List[str] = Field(
         [],
         title="create the given list of tags on datasets",
     )
@@ -76,7 +78,7 @@ class LibraryContentsCreatePayload(Model):
         None,
         title="(only if create_type is 'file') the encoded id of an accessible HDCA to copy into the library",
     )
-    ldda_message: Optional[str] = Field(
+    ldda_message: str = Field(
         "",
         title="the new message attribute of the LDDA created",
     )
@@ -85,13 +87,20 @@ class LibraryContentsCreatePayload(Model):
         title="sub-dictionary containing any extended metadata to associate with the item",
     )
 
+    @field_validator("tags", mode="before", check_fields=False)
+    @classmethod
+    def tags_string_to_json(cls, v):
+        if isinstance(v, str):
+            return json.loads(v)
+        return v
+
 
 class LibraryContentsFileCreatePayload(LibraryContentsCreatePayload):
-    dbkey: Optional[Union[str, list]] = Field(
+    dbkey: Union[str, list] = Field(
         "?",
         title="database key",
     )
-    roles: Optional[str] = Field(
+    roles: str = Field(
         "",
         title="user selected roles",
     )
@@ -99,7 +108,7 @@ class LibraryContentsFileCreatePayload(LibraryContentsCreatePayload):
         None,
         title="file type",
     )
-    server_dir: Optional[str] = Field(
+    server_dir: str = Field(
         "",
         title="(only if upload_option is 'upload_directory') relative path of the "
         "subdirectory of Galaxy ``library_import_dir`` (if admin) or "
@@ -107,12 +116,12 @@ class LibraryContentsFileCreatePayload(LibraryContentsCreatePayload):
         "All and only the files (i.e. no subdirectories) contained "
         "in the specified directory will be uploaded.",
     )
-    filesystem_paths: Optional[str] = Field(
+    filesystem_paths: str = Field(
         "",
         title="(only if upload_option is 'upload_paths' and the user is an admin) "
         "file paths on the Galaxy server to upload to the library, one file per line",
     )
-    link_data_only: Optional[LinkDataOnly] = Field(
+    link_data_only: LinkDataOnly = Field(
         LinkDataOnly.copy_files,
         title="(only when upload_option is 'upload_directory' or 'upload_paths')."
         "Setting to 'link_to_files' symlinks instead of copying the files",
@@ -122,13 +131,16 @@ class LibraryContentsFileCreatePayload(LibraryContentsCreatePayload):
         title="UUID of the dataset to upload",
     )
 
+    # uploaded file fields
+    model_config = ConfigDict(extra="allow")
+
 
 class LibraryContentsFolderCreatePayload(LibraryContentsCreatePayload):
-    name: Optional[str] = Field(
+    name: str = Field(
         "",
         title="name of the folder to create",
     )
-    description: Optional[str] = Field(
+    description: str = Field(
         "",
         title="description of the folder to create",
     )
@@ -147,11 +159,11 @@ class LibraryContentsCollectionCreatePayload(LibraryContentsCreatePayload):
         None,
         title="the name of the collection",
     )
-    hide_source_items: Optional[bool] = Field(
+    hide_source_items: bool = Field(
         False,
         title="if True, hide the source items in the collection",
     )
-    copy_elements: Optional[bool] = Field(
+    copy_elements: bool = Field(
         False,
         title="if True, copy the elements into the collection",
     )
@@ -165,7 +177,7 @@ class LibraryContentsUpdatePayload(Model):
 
 
 class LibraryContentsDeletePayload(Model):
-    purge: Optional[bool] = Field(
+    purge: bool = Field(
         False,
         title="if True, purge the library dataset",
     )
diff --git a/lib/galaxy/webapps/galaxy/api/library_contents.py b/lib/galaxy/webapps/galaxy/api/library_contents.py
index 566744599fae..53a03dc3f3af 100644
--- a/lib/galaxy/webapps/galaxy/api/library_contents.py
+++ b/lib/galaxy/webapps/galaxy/api/library_contents.py
@@ -3,12 +3,22 @@
 """
 
 import logging
+import shutil
+import tempfile
 from typing import (
+    List,
     Optional,
     Union,
 )
 
-from fastapi import Body
+from fastapi import (
+    Body,
+    Depends,
+    Request,
+    UploadFile,
+)
+from pydantic import Json
+from starlette.datastructures import UploadFile as StarletteUploadFile
 
 from galaxy.managers.context import (
     ProvidesHistoryContext,
@@ -41,12 +51,27 @@
     LibraryContentsService,
     MaybeLibraryFolderOrDatasetID,
 )
+from . import (
+    APIContentTypeRoute,
+    as_form,
+)
 
 log = logging.getLogger(__name__)
 
 router = Router(tags=["libraries"])
 
 
+class FormDataApiRoute(APIContentTypeRoute):
+    match_content_type = "multipart/form-data"
+
+
+class JsonApiRoute(APIContentTypeRoute):
+    match_content_type = "application/json"
+
+
+LibraryContentsCreateForm = as_form(LibraryContentsFileCreatePayload)
+
+
 @router.cbv
 class FastAPILibraryContents:
     service: LibraryContentsService = depends(LibraryContentsService)
@@ -90,13 +115,40 @@ def show(
         "/api/libraries/{library_id}/contents",
         summary="Create a new library file or folder.",
         deprecated=True,
+        route_class_override=JsonApiRoute,
     )
-    def create(
+    def create_json(
         self,
         library_id: Union[DecodedDatabaseIdField, LibraryFolderDatabaseIdField],
         payload: Union[
             LibraryContentsFolderCreatePayload, LibraryContentsFileCreatePayload, LibraryContentsCollectionCreatePayload
-        ],
+        ] = Body(...),
+        trans: ProvidesHistoryContext = DependsOnTrans,
+    ) -> Union[
+        LibraryContentsCreateFolderListResponse,
+        LibraryContentsCreateFileListResponse,
+        LibraryContentsCreateDatasetCollectionResponse,
+        LibraryContentsCreateDatasetResponse,
+    ]:
+        """
+        This endpoint is deprecated. Please use POST /api/folders/{folder_id} or POST /api/folders/{folder_id}/contents instead.
+        """
+        return self.service.create(trans, library_id, payload)
+
+    @router.post(
+        "/api/libraries/{library_id}/contents",
+        summary="Create a new library file or folder.",
+        deprecated=True,
+        route_class_override=FormDataApiRoute,
+    )
+    async def create_form(
+        self,
+        request: Request,
+        library_id: Union[DecodedDatabaseIdField, LibraryFolderDatabaseIdField],
+        payload: Union[Json[LibraryContentsFileCreatePayload], LibraryContentsFileCreatePayload] = Depends(
+            LibraryContentsCreateForm.as_form
+        ),
+        files: Optional[List[UploadFile]] = None,
         trans: ProvidesHistoryContext = DependsOnTrans,
     ) -> Union[
         LibraryContentsCreateFolderListResponse,
@@ -107,6 +159,20 @@ def create(
         """
         This endpoint is deprecated. Please use POST /api/folders/{folder_id} or POST /api/folders/{folder_id}/contents instead.
         """
+        # FastAPI's UploadFile is a very light wrapper around starlette's UploadFile
+        if not files:
+            data = await request.form()
+            upload_files = []
+            for i, upload_file in enumerate(data.values()):
+                if isinstance(upload_file, StarletteUploadFile):
+                    with tempfile.NamedTemporaryFile(
+                        dir=trans.app.config.new_file_path, prefix="upload_file_data_", delete=False
+                    ) as dest:
+                        shutil.copyfileobj(upload_file.file, dest)  # type: ignore[misc]  # https://github.com/python/mypy/issues/15031
+                    upload_file.file.close()
+                    upload_files.append(dict(filename=upload_file.filename, local_filename=dest.name))
+            setattr(payload, "files", upload_files)
+
         return self.service.create(trans, library_id, payload)
 
     @router.put(
diff --git a/lib/galaxy_test/api/test_tags.py b/lib/galaxy_test/api/test_tags.py
index 035f675aecb5..cdce0a0705af 100644
--- a/lib/galaxy_test/api/test_tags.py
+++ b/lib/galaxy_test/api/test_tags.py
@@ -114,7 +114,9 @@ def _get_item(self, item_id: str):
 
     def test_upload_file_contents_with_tags(self):
         initial_tags = ["name:foobar", "barfoo"]
-        ld = self.library_populator.new_library_dataset(name=f"test-library-dataset-{uuid4()}", tags=initial_tags)
+        ld = self.library_populator.new_library_dataset(
+            name=f"test-library-dataset-{uuid4()}", tags=json.dumps(initial_tags)
+        )
         assert ld["tags"] == initial_tags
 
 
diff --git a/lib/galaxy_test/base/populators.py b/lib/galaxy_test/base/populators.py
index abd8fe1b5a24..82b458d0068e 100644
--- a/lib/galaxy_test/base/populators.py
+++ b/lib/galaxy_test/base/populators.py
@@ -2740,7 +2740,7 @@ def raw_library_contents_create(self, library_id, payload, files=None):
             files = {}
 
         url_rel = f"libraries/{library_id}/contents"
-        return self.galaxy_interactor.post(url_rel, payload, files=files, json=True)
+        return self.galaxy_interactor.post(url_rel, payload, files=files)
 
     def show_ld_raw(self, library_id: str, library_dataset_id: str) -> Response:
         response = self.galaxy_interactor.get(f"libraries/{library_id}/contents/{library_dataset_id}")
@@ -2759,9 +2759,7 @@ def show_ldda(self, ldda_id):
     def new_library_dataset_in_private_library(self, library_name="private_dataset", wait=True):
         library = self.new_private_library(library_name)
         payload, files = self.create_dataset_request(library, file_type="txt", contents="create_test")
-        create_response = self.galaxy_interactor.post(
-            f"libraries/{library['id']}/contents", payload, files=files, json=True
-        )
+        create_response = self.galaxy_interactor.post(f"libraries/{library['id']}/contents", payload, files=files)
         api_asserts.assert_status_code_is(create_response, 200)
         library_datasets = create_response.json()
         assert len(library_datasets) == 1