diff --git a/cli/templateedit_test.go b/cli/templateedit_test.go
index 23b181391b90d..558839de2c9d6 100644
--- a/cli/templateedit_test.go
+++ b/cli/templateedit_test.go
@@ -218,8 +218,9 @@ func TestTemplateEdit(t *testing.T) {
 		// Properties don't change
 		assert.Equal(t, template.Name, updated.Name)
 		assert.Equal(t, template.Description, updated.Description)
-		assert.Equal(t, template.DisplayName, updated.DisplayName)
-		// Icon is removed, as the API considers it as "delete" request
+		// These properties are removed, as the API considers it as "delete" request
+		// See: https://github.com/coder/coder/issues/5066
 		assert.Equal(t, "", updated.Icon)
+		assert.Equal(t, "", updated.DisplayName)
 	})
 }
diff --git a/coderd/templates.go b/coderd/templates.go
index d7cdef2a1b123..7f27fb7c2f882 100644
--- a/coderd/templates.go
+++ b/coderd/templates.go
@@ -480,7 +480,9 @@ func (api *API) patchTemplateMeta(rw http.ResponseWriter, r *http.Request) {
 			return nil
 		}
 
-		// Update template metadata -- empty fields are not overwritten.
+		// Update template metadata -- empty fields are not overwritten,
+		// except for display_name, icon, and default_ttl.
+		// The exception is required to clear content of these fields with UI.
 		name := req.Name
 		displayName := req.DisplayName
 		desc := req.Description
@@ -490,9 +492,6 @@ func (api *API) patchTemplateMeta(rw http.ResponseWriter, r *http.Request) {
 		if name == "" {
 			name = template.Name
 		}
-		if displayName == "" {
-			displayName = template.DisplayName
-		}
 		if desc == "" {
 			desc = template.Description
 		}
diff --git a/site/src/components/TemplateLayout/TemplateLayout.tsx b/site/src/components/TemplateLayout/TemplateLayout.tsx
index 7567d572207ef..04bb2d404f364 100644
--- a/site/src/components/TemplateLayout/TemplateLayout.tsx
+++ b/site/src/components/TemplateLayout/TemplateLayout.tsx
@@ -151,9 +151,12 @@ export const TemplateLayout: FC<PropsWithChildren> = ({ children }) => {
                 </Avatar>
               )}
             </div>
-
             <div>
-              <PageHeaderTitle>{template.name}</PageHeaderTitle>
+              <PageHeaderTitle>
+                {template.display_name.length > 0
+                  ? template.display_name
+                  : template.name}
+              </PageHeaderTitle>
               <PageHeaderSubtitle condensed>
                 {template.description === ""
                   ? Language.noDescription
diff --git a/site/src/i18n/en/templatePage.json b/site/src/i18n/en/templatePage.json
index fcbf8541dc492..8c78adf849901 100644
--- a/site/src/i18n/en/templatePage.json
+++ b/site/src/i18n/en/templatePage.json
@@ -9,5 +9,6 @@
       "deleteTemplateCaption": "Once you delete a template, there is no going back. Please be certain.",
       "deleteCta": "Delete Template"
     }
-  }
+  },
+  "displayNameLabel": "Display name"
 }
diff --git a/site/src/pages/CreateWorkspacePage/CreateWorkspacePageView.tsx b/site/src/pages/CreateWorkspacePage/CreateWorkspacePageView.tsx
index 610603f5fb35a..ed9562351167d 100644
--- a/site/src/pages/CreateWorkspacePage/CreateWorkspacePageView.tsx
+++ b/site/src/pages/CreateWorkspacePage/CreateWorkspacePageView.tsx
@@ -182,7 +182,9 @@ export const CreateWorkspacePageView: FC<
                   </div>
                   <Stack direction="column" spacing={0.5}>
                     <span className={styles.templateName}>
-                      {props.selectedTemplate.name}
+                      {props.selectedTemplate.display_name.length > 0
+                        ? props.selectedTemplate.display_name
+                        : props.selectedTemplate.name}
                     </span>
                     {props.selectedTemplate.description && (
                       <span className={styles.templateDescription}>
diff --git a/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.test.tsx b/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.test.tsx
index cc36c9595930d..bd2ab35e06ba2 100644
--- a/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.test.tsx
+++ b/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.test.tsx
@@ -37,7 +37,7 @@ describe("TemplateSummaryPage", () => {
     mock.mockImplementation(() => "a minute ago")
 
     renderPage()
-    await screen.findByText(MockTemplate.name)
+    await screen.findByText(MockTemplate.display_name)
     await screen.findByTestId("markdown")
     screen.getByText(MockWorkspaceResource.name)
     screen.queryAllByText(`${MockTemplateVersion.name}`).length
diff --git a/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.tsx b/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.tsx
index 7155f1b2d4354..42cbd7dd63ae8 100644
--- a/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.tsx
+++ b/site/src/pages/TemplatePage/TemplateSummaryPage/TemplateSummaryPage.tsx
@@ -22,7 +22,15 @@ export const TemplateSummaryPage: FC = () => {
   return (
     <>
       <Helmet>
-        <title>{pageTitle(`${template.name} · Template`)}</title>
+        <title>
+          {pageTitle(
+            `${
+              template.display_name.length > 0
+                ? template.display_name
+                : template.name
+            } · Template`,
+          )}
+        </title>
       </Helmet>
       <TemplateSummaryPageView
         template={template}
diff --git a/site/src/pages/TemplateSettingsPage/TemplateSettingsForm.tsx b/site/src/pages/TemplateSettingsPage/TemplateSettingsForm.tsx
index 4c03bfa49d2af..14e0aa07594c1 100644
--- a/site/src/pages/TemplateSettingsPage/TemplateSettingsForm.tsx
+++ b/site/src/pages/TemplateSettingsPage/TemplateSettingsForm.tsx
@@ -12,8 +12,15 @@ import { Stack } from "components/Stack/Stack"
 import { FormikContextType, FormikTouched, useFormik } from "formik"
 import { FC, useRef, useState } from "react"
 import { colors } from "theme/colors"
-import { getFormHelpers, nameValidator, onChangeTrimmed } from "util/formUtils"
+import {
+  getFormHelpers,
+  nameValidator,
+  templateDisplayNameValidator,
+  onChangeTrimmed,
+} from "util/formUtils"
 import * as Yup from "yup"
+import i18next from "i18next"
+import { useTranslation } from "react-i18next"
 
 export const Language = {
   nameLabel: "Name",
@@ -36,6 +43,11 @@ const MS_HOUR_CONVERSION = 3600000
 
 export const validationSchema = Yup.object({
   name: nameValidator(Language.nameLabel),
+  display_name: templateDisplayNameValidator(
+    i18next.t("displayNameLabel", {
+      ns: "templatePage",
+    }),
+  ),
   description: Yup.string().max(
     MAX_DESCRIPTION_CHAR_LIMIT,
     Language.descriptionMaxError,
@@ -92,6 +104,8 @@ export const TemplateSettingsForm: FC<TemplateSettingsForm> = ({
   const hasIcon = form.values.icon && form.values.icon !== ""
   const emojiButtonRef = useRef<HTMLButtonElement>(null)
 
+  const { t } = useTranslation("templatePage")
+
   return (
     <form onSubmit={form.handleSubmit} aria-label={Language.formAriaLabel}>
       <Stack>
@@ -105,6 +119,14 @@ export const TemplateSettingsForm: FC<TemplateSettingsForm> = ({
           variant="outlined"
         />
 
+        <TextField
+          {...getFieldHelpers("display_name")}
+          disabled={isSubmitting}
+          fullWidth
+          label={t("displayNameLabel")}
+          variant="outlined"
+        />
+
         <TextField
           {...getFieldHelpers("description")}
           multiline
diff --git a/site/src/pages/TemplateSettingsPage/TemplateSettingsPage.test.tsx b/site/src/pages/TemplateSettingsPage/TemplateSettingsPage.test.tsx
index 9690f7c5ecea9..ea4effe0fbdbb 100644
--- a/site/src/pages/TemplateSettingsPage/TemplateSettingsPage.test.tsx
+++ b/site/src/pages/TemplateSettingsPage/TemplateSettingsPage.test.tsx
@@ -24,7 +24,7 @@ const renderTemplateSettingsPage = async () => {
 
 const validFormValues = {
   name: "Name",
-  display_name: "Test Template",
+  display_name: "A display name",
   description: "A description",
   icon: "A string",
   default_ttl_ms: 1,
@@ -32,6 +32,7 @@ const validFormValues = {
 
 const fillAndSubmitForm = async ({
   name,
+  display_name,
   description,
   default_ttl_ms,
   icon,
@@ -40,6 +41,15 @@ const fillAndSubmitForm = async ({
   await userEvent.clear(nameField)
   await userEvent.type(nameField, name)
 
+  const { t } = i18next
+  const displayNameLabel = t("displayNameLabel", {
+    ns: "templatePage",
+  })
+
+  const displayNameField = await screen.findByLabelText(displayNameLabel)
+  await userEvent.clear(displayNameField)
+  await userEvent.type(displayNameField, display_name)
+
   const descriptionField = await screen.findByLabelText(
     FormLanguage.descriptionLabel,
   )
diff --git a/site/src/pages/TemplatesPage/TemplatesPage.test.tsx b/site/src/pages/TemplatesPage/TemplatesPage.test.tsx
index 16cffb1ff8f27..d06091976481e 100644
--- a/site/src/pages/TemplatesPage/TemplatesPage.test.tsx
+++ b/site/src/pages/TemplatesPage/TemplatesPage.test.tsx
@@ -46,7 +46,7 @@ describe("TemplatesPage", () => {
     render(<TemplatesPage />)
 
     // Then
-    await screen.findByText(MockTemplate.name)
+    await screen.findByText(MockTemplate.display_name)
   })
 
   it("shows empty view without permissions to create", async () => {
diff --git a/site/src/pages/TemplatesPage/TemplatesPageView.tsx b/site/src/pages/TemplatesPage/TemplatesPageView.tsx
index cbfe68d55039c..0a5d103534f5a 100644
--- a/site/src/pages/TemplatesPage/TemplatesPageView.tsx
+++ b/site/src/pages/TemplatesPage/TemplatesPageView.tsx
@@ -209,7 +209,11 @@ export const TemplatesPageView: FC<
                         >
                           <TableCellLink to={templatePageLink}>
                             <AvatarData
-                              title={template.name}
+                              title={
+                                template.display_name.length > 0
+                                  ? template.display_name
+                                  : template.name
+                              }
                               subtitle={template.description}
                               highlightTitle
                               avatar={
diff --git a/site/src/util/formUtils.ts b/site/src/util/formUtils.ts
index ab411143f7718..790e070341c5c 100644
--- a/site/src/util/formUtils.ts
+++ b/site/src/util/formUtils.ts
@@ -19,8 +19,11 @@ export const Language = {
   nameInvalidChars: (name: string): string => {
     return `${name} must start with a-Z or 0-9 and can contain a-Z, 0-9 or -`
   },
-  nameTooLong: (name: string): string => {
-    return `${name} cannot be longer than 32 characters`
+  nameTooLong: (name: string, len: number): string => {
+    return `${name} cannot be longer than ${len} characters`
+  },
+  templateDisplayNameInvalidChars: (name: string): string => {
+    return `${name} must start and end with non-whitespace character`
   },
 }
 
@@ -74,15 +77,28 @@ export const onChangeTrimmed =
     form.handleChange(event)
   }
 
-// REMARK: Keep in sync with coderd/httpapi/httpapi.go#L40
+// REMARK: Keep these consts in sync with coderd/httpapi/httpapi.go
 const maxLenName = 32
-
-// REMARK: Keep in sync with coderd/httpapi/httpapi.go#L18
+const templateDisplayNameMaxLength = 64
 const usernameRE = /^[a-zA-Z0-9]+(?:-[a-zA-Z0-9]+)*$/
+const templateDisplayNameRE = /^[^\s](.*[^\s])?$/
 
 // REMARK: see #1756 for name/username semantics
 export const nameValidator = (name: string): Yup.StringSchema =>
   Yup.string()
     .required(Language.nameRequired(name))
     .matches(usernameRE, Language.nameInvalidChars(name))
-    .max(maxLenName, Language.nameTooLong(name))
+    .max(maxLenName, Language.nameTooLong(name, maxLenName))
+
+export const templateDisplayNameValidator = (
+  displayName: string,
+): Yup.StringSchema =>
+  Yup.string()
+    .matches(
+      templateDisplayNameRE,
+      Language.templateDisplayNameInvalidChars(displayName),
+    )
+    .max(
+      templateDisplayNameMaxLength,
+      Language.nameTooLong(displayName, templateDisplayNameMaxLength),
+    )