diff --git a/site/src/pages/TemplatePage/TemplateRedirectController.test.tsx b/site/src/pages/TemplatePage/TemplateRedirectController.test.tsx
new file mode 100644
index 0000000000000..459e94fe911f0
--- /dev/null
+++ b/site/src/pages/TemplatePage/TemplateRedirectController.test.tsx
@@ -0,0 +1,40 @@
+import { waitFor } from "@testing-library/react";
+import { API } from "api/api";
+import * as M from "testHelpers/entities";
+import { renderWithAuth } from "testHelpers/renderHelpers";
+import { TemplateRedirectController } from "./TemplateRedirectController";
+
+const renderTemplateRedirectController = (route: string) => {
+  return renderWithAuth(<TemplateRedirectController />, {
+    route,
+    path: "/templates/:organization?/:template",
+  });
+};
+
+it("redirects from multi-org to single-org", async () => {
+  const { router } = renderTemplateRedirectController(
+    `/templates/${M.MockTemplate.organization_name}/${M.MockTemplate.name}`,
+  );
+
+  await waitFor(() =>
+    expect(router.state.location.pathname).toEqual(
+      `/templates/${M.MockTemplate.name}`,
+    ),
+  );
+});
+
+it("redirects from single-org to multi-org", async () => {
+  jest
+    .spyOn(API, "getOrganizations")
+    .mockResolvedValueOnce([M.MockDefaultOrganization, M.MockOrganization2]);
+
+  const { router } = renderTemplateRedirectController(
+    `/templates/${M.MockTemplate.name}`,
+  );
+
+  await waitFor(() =>
+    expect(router.state.location.pathname).toEqual(
+      `/templates/${M.MockDefaultOrganization.name}/${M.MockTemplate.name}`,
+    ),
+  );
+});
diff --git a/site/src/pages/TemplatePage/TemplateRedirectController.tsx b/site/src/pages/TemplatePage/TemplateRedirectController.tsx
new file mode 100644
index 0000000000000..66da3b6ea0bab
--- /dev/null
+++ b/site/src/pages/TemplatePage/TemplateRedirectController.tsx
@@ -0,0 +1,53 @@
+import type { FC } from "react";
+import { Navigate, Outlet, useLocation, useParams } from "react-router-dom";
+import type { Organization } from "api/typesGenerated";
+import { useDashboard } from "modules/dashboard/useDashboard";
+
+export const TemplateRedirectController: FC = () => {
+  const { organizations, showOrganizations } = useDashboard();
+  const { organization, template } = useParams() as {
+    organization?: string;
+    template: string;
+  };
+  const location = useLocation();
+
+  // We redirect templates without an organization to the default organization,
+  // as that's likely what any links floating around expect.
+  if (showOrganizations && !organization) {
+    const extraPath = removePrefix(location.pathname, `/templates/${template}`);
+
+    return (
+      <Navigate
+        to={`/templates/${getOrganizationNameByDefault(
+          organizations,
+        )}/${template}${extraPath}${location.search}`}
+        replace
+      />
+    );
+  }
+
+  // `showOrganizations` can only be false when there is a single organization,
+  // so it's safe to throw away the organization name.
+  if (!showOrganizations && organization) {
+    const extraPath = removePrefix(
+      location.pathname,
+      `/templates/${organization}/${template}`,
+    );
+
+    return (
+      <Navigate
+        to={`/templates/${template}${extraPath}${location.search}`}
+        replace
+      />
+    );
+  }
+
+  return <Outlet />;
+};
+
+const getOrganizationNameByDefault = (organizations: Organization[]) =>
+  organizations.find((org) => org.is_default)?.name;
+
+// I really hate doing it this way, but React Router does not provide a better way.
+const removePrefix = (self: string, prefix: string) =>
+  self.startsWith(prefix) ? self.slice(prefix.length) : self;
diff --git a/site/src/router.tsx b/site/src/router.tsx
index 152c458b83fb4..75091a311cb3a 100644
--- a/site/src/router.tsx
+++ b/site/src/router.tsx
@@ -1,4 +1,4 @@
-import { Suspense, lazy } from "react";
+import { lazy, Suspense } from "react";
 import {
   createBrowserRouter,
   createRoutesFromChildren,
@@ -6,6 +6,7 @@ import {
   Outlet,
   Route,
 } from "react-router-dom";
+import { TemplateRedirectController } from "pages/TemplatePage/TemplateRedirectController";
 import { Loader } from "./components/Loader/Loader";
 import { RequireAuth } from "./contexts/auth/RequireAuth";
 import { DashboardLayout } from "./modules/dashboard/DashboardLayout";
@@ -289,27 +290,29 @@ const RoutesWithSuspense = () => {
 const templateRouter = () => {
   return (
     <Route path=":template">
-      <Route element={<TemplateLayout />}>
-        <Route index element={<TemplateSummaryPage />} />
-        <Route path="docs" element={<TemplateDocsPage />} />
-        <Route path="files" element={<TemplateFilesPage />} />
-        <Route path="versions" element={<TemplateVersionsPage />} />
-        <Route path="embed" element={<TemplateEmbedPage />} />
-        <Route path="insights" element={<TemplateInsightsPage />} />
-      </Route>
+      <Route element={<TemplateRedirectController />}>
+        <Route element={<TemplateLayout />}>
+          <Route index element={<TemplateSummaryPage />} />
+          <Route path="docs" element={<TemplateDocsPage />} />
+          <Route path="files" element={<TemplateFilesPage />} />
+          <Route path="versions" element={<TemplateVersionsPage />} />
+          <Route path="embed" element={<TemplateEmbedPage />} />
+          <Route path="insights" element={<TemplateInsightsPage />} />
+        </Route>
 
-      <Route path="workspace" element={<CreateWorkspacePage />} />
+        <Route path="workspace" element={<CreateWorkspacePage />} />
 
-      <Route path="settings" element={<TemplateSettingsLayout />}>
-        <Route index element={<TemplateSettingsPage />} />
-        <Route path="permissions" element={<TemplatePermissionsPage />} />
-        <Route path="variables" element={<TemplateVariablesPage />} />
-        <Route path="schedule" element={<TemplateSchedulePage />} />
-      </Route>
+        <Route path="settings" element={<TemplateSettingsLayout />}>
+          <Route index element={<TemplateSettingsPage />} />
+          <Route path="permissions" element={<TemplatePermissionsPage />} />
+          <Route path="variables" element={<TemplateVariablesPage />} />
+          <Route path="schedule" element={<TemplateSchedulePage />} />
+        </Route>
 
-      <Route path="versions">
-        <Route path=":version">
-          <Route index element={<TemplateVersionPage />} />
+        <Route path="versions">
+          <Route path=":version">
+            <Route index element={<TemplateVersionPage />} />
+          </Route>
         </Route>
       </Route>
     </Route>