diff --git a/.eslintrc.json b/.eslintrc.json
index ef9c8a183f..3d56f5861f 100644
--- a/.eslintrc.json
+++ b/.eslintrc.json
@@ -99,7 +99,6 @@
                 "$": false,
                 "FetchStatus": false,
                 "Filter": false,
-                "Handlebars": false,
                 "LightboxCanvas": false,
                 "ListCursor": false,
                 "MessageListData": false,
diff --git a/frontend_tests/node_tests/activity.js b/frontend_tests/node_tests/activity.js
index a8176028c5..ae139374b9 100644
--- a/frontend_tests/node_tests/activity.js
+++ b/frontend_tests/node_tests/activity.js
@@ -75,7 +75,6 @@ set_global("stream_popover", _stream_popover);
 set_global("ui", _ui);
 
 zrequire("compose_fade");
-set_global("Handlebars", global.make_handlebars());
 zrequire("unread");
 zrequire("hash_util");
 zrequire("narrow");
diff --git a/frontend_tests/node_tests/compose.js b/frontend_tests/node_tests/compose.js
index b1ae9fb5ca..d1d0b6c052 100644
--- a/frontend_tests/node_tests/compose.js
+++ b/frontend_tests/node_tests/compose.js
@@ -67,7 +67,6 @@ zrequire("compose_ui");
 const util = zrequire("util");
 zrequire("rtl");
 zrequire("common");
-set_global("Handlebars", global.make_handlebars());
 zrequire("stream_data");
 zrequire("compose_state");
 zrequire("people");
diff --git a/frontend_tests/node_tests/composebox_typeahead.js b/frontend_tests/node_tests/composebox_typeahead.js
index d78682abde..2b4ccec0a4 100644
--- a/frontend_tests/node_tests/composebox_typeahead.js
+++ b/frontend_tests/node_tests/composebox_typeahead.js
@@ -2,7 +2,6 @@ const emoji = zrequire("emoji", "shared/js/emoji");
 const typeahead = zrequire("typeahead", "shared/js/typeahead");
 zrequire("compose_state");
 zrequire("pm_conversations");
-set_global("Handlebars", global.make_handlebars());
 zrequire("templates");
 zrequire("typeahead_helper");
 zrequire("people");
diff --git a/frontend_tests/node_tests/drafts.js b/frontend_tests/node_tests/drafts.js
index 41c39b19bb..5e03fb09e1 100644
--- a/frontend_tests/node_tests/drafts.js
+++ b/frontend_tests/node_tests/drafts.js
@@ -5,7 +5,6 @@ set_global("$", global.make_zjquery());
 zrequire("localstorage");
 zrequire("drafts");
 zrequire("timerender");
-set_global("Handlebars", global.make_handlebars());
 zrequire("stream_color");
 zrequire("colorspace");
 
diff --git a/frontend_tests/node_tests/filter.js b/frontend_tests/node_tests/filter.js
index 903b0cac81..6247f8477b 100644
--- a/frontend_tests/node_tests/filter.js
+++ b/frontend_tests/node_tests/filter.js
@@ -1,7 +1,6 @@
 zrequire("unread");
 zrequire("stream_data");
 zrequire("people");
-set_global("Handlebars", global.make_handlebars());
 global.stub_out_jquery();
 set_global("$", global.make_zjquery());
 zrequire("message_util", "js/message_util");
diff --git a/frontend_tests/node_tests/i18n.js b/frontend_tests/node_tests/i18n.js
index 3cb745b068..23616fee5c 100644
--- a/frontend_tests/node_tests/i18n.js
+++ b/frontend_tests/node_tests/i18n.js
@@ -1,4 +1,3 @@
-set_global("Handlebars", global.make_handlebars());
 zrequire("templates");
 
 // We download our translations in `page_params` (which
diff --git a/frontend_tests/node_tests/input_pill.js b/frontend_tests/node_tests/input_pill.js
index d677dd4dcb..aef52736c3 100644
--- a/frontend_tests/node_tests/input_pill.js
+++ b/frontend_tests/node_tests/input_pill.js
@@ -1,7 +1,6 @@
 set_global("$", global.make_zjquery());
 zrequire("input_pill");
 
-set_global("Handlebars", global.make_handlebars());
 zrequire("templates");
 
 set_global("document", {});
diff --git a/frontend_tests/node_tests/search_pill.js b/frontend_tests/node_tests/search_pill.js
index 200c60d524..b26776af02 100644
--- a/frontend_tests/node_tests/search_pill.js
+++ b/frontend_tests/node_tests/search_pill.js
@@ -1,7 +1,6 @@
 zrequire("search_pill");
 zrequire("input_pill");
 zrequire("Filter", "js/filter");
-set_global("Handlebars", global.make_handlebars());
 
 const is_starred_item = {
     display_value: "is:starred",
diff --git a/frontend_tests/node_tests/search_suggestion.js b/frontend_tests/node_tests/search_suggestion.js
index 7ca20e0762..5bb1cbd590 100644
--- a/frontend_tests/node_tests/search_suggestion.js
+++ b/frontend_tests/node_tests/search_suggestion.js
@@ -13,7 +13,6 @@ page_params.realm_email_address_visibility =
 const huddle_data = zrequire("huddle_data");
 
 zrequire("typeahead_helper");
-set_global("Handlebars", global.make_handlebars());
 zrequire("Filter", "js/filter");
 zrequire("narrow_state");
 zrequire("stream_data");
diff --git a/frontend_tests/node_tests/search_suggestion_legacy.js b/frontend_tests/node_tests/search_suggestion_legacy.js
index 92d693d40e..301502879b 100644
--- a/frontend_tests/node_tests/search_suggestion_legacy.js
+++ b/frontend_tests/node_tests/search_suggestion_legacy.js
@@ -12,7 +12,6 @@ page_params.realm_email_address_visibility =
 const huddle_data = zrequire("huddle_data");
 
 zrequire("typeahead_helper");
-set_global("Handlebars", global.make_handlebars());
 zrequire("Filter", "js/filter");
 zrequire("narrow_state");
 zrequire("stream_data");
diff --git a/frontend_tests/node_tests/typeahead_helper.js b/frontend_tests/node_tests/typeahead_helper.js
index 5354617ec1..a1911f766c 100644
--- a/frontend_tests/node_tests/typeahead_helper.js
+++ b/frontend_tests/node_tests/typeahead_helper.js
@@ -5,7 +5,6 @@ const settings_config = zrequire("settings_config");
 page_params.realm_email_address_visibility =
     settings_config.email_address_visibility_values.admins_only.code;
 
-set_global("Handlebars", global.make_handlebars());
 zrequire("recent_senders");
 zrequire("pm_conversations");
 zrequire("people");
diff --git a/frontend_tests/zjsunit/handlebars.js b/frontend_tests/zjsunit/handlebars.js
index a1a5d8d490..9daafc87e2 100644
--- a/frontend_tests/zjsunit/handlebars.js
+++ b/frontend_tests/zjsunit/handlebars.js
@@ -1,13 +1,11 @@
 const fs = require("fs");
 const path = require("path");
 
-const Handlebars = require("handlebars/dist/cjs/handlebars.js");
+const Handlebars = require("handlebars");
 const {SourceMapConsumer, SourceNode} = require("source-map");
 
 const templates_path = path.resolve(__dirname, "../../static/templates");
 
-exports.make_handlebars = () => Handlebars.create();
-
 exports.stub_templates = (stub) => {
     window.template_stub = stub;
 };
@@ -34,18 +32,16 @@ require.extensions[".hbs"] = (module, filename) => {
     const pc = hb.precompile(code, {preventIndent: true, srcName: filename});
     const node = new SourceNode();
     node.add([
-        "let hb, template;\n",
+        'const Handlebars = require("handlebars/runtime");\n',
+        "const template = Handlebars.template(",
+        SourceNode.fromStringWithSourceMap(pc.code, new SourceMapConsumer(pc.map)),
+        ");\n",
         "module.exports = (...args) => {\n",
         "    if (window.template_stub !== undefined) {\n",
         "        return window.template_stub(",
         JSON.stringify(name),
         ", ...args);\n",
         "    }\n",
-        "    if (hb !== Handlebars) {\n",
-        "        template = (hb = Handlebars).template(",
-        SourceNode.fromStringWithSourceMap(pc.code, new SourceMapConsumer(pc.map)),
-        ");\n",
-        "    }\n",
         "    return template(...args);\n",
         "};\n",
     ]);
diff --git a/frontend_tests/zjsunit/index.js b/frontend_tests/zjsunit/index.js
index 1fa70d006a..6cfdb072c0 100644
--- a/frontend_tests/zjsunit/index.js
+++ b/frontend_tests/zjsunit/index.js
@@ -2,6 +2,7 @@ const fs = require("fs");
 const Module = require("module");
 const path = require("path");
 
+const Handlebars = require("handlebars/runtime");
 const _ = require("lodash");
 
 const finder = require("./finder.js");
@@ -57,7 +58,6 @@ global.with_stub = stub.with_stub;
 global.make_zjquery = zjquery.make_zjquery;
 
 // Set up Handlebars
-global.make_handlebars = handlebars.make_handlebars;
 global.stub_templates = handlebars.stub_templates;
 
 const noop = function () {};
@@ -136,6 +136,7 @@ try {
         }
 
         namespace.restore();
+        Handlebars.HandlebarsEnvironment();
     });
 } catch (e) {
     if (e.stack) {
diff --git a/static/js/bundles/app.js b/static/js/bundles/app.js
index 1639e361c4..90c85c5278 100644
--- a/static/js/bundles/app.js
+++ b/static/js/bundles/app.js
@@ -7,7 +7,6 @@ import "jquery-caret-plugin/src/jquery.caret.js";
 import "../../third/jquery-idle/jquery.idle.js";
 import "spectrum-colorpicker";
 import "jquery-validation/dist/jquery.validate.js";
-import "handlebars/dist/cjs/handlebars.runtime.js";
 import "flatpickr/dist/flatpickr.js";
 import "flatpickr/dist/plugins/confirmDate/confirmDate.js";
 
diff --git a/static/js/compose.js b/static/js/compose.js
index 9b3a8bcfc5..00ecb4c71c 100644
--- a/static/js/compose.js
+++ b/static/js/compose.js
@@ -1,3 +1,5 @@
+const Handlebars = require("handlebars/runtime");
+
 const render_compose_all_everyone = require("../templates/compose_all_everyone.hbs");
 const render_compose_announce = require("../templates/compose_announce.hbs");
 const render_compose_invite_users = require("../templates/compose_invite_users.hbs");
diff --git a/static/js/drafts.js b/static/js/drafts.js
index 848403cde7..f4f491416f 100644
--- a/static/js/drafts.js
+++ b/static/js/drafts.js
@@ -1,3 +1,4 @@
+const Handlebars = require("handlebars/runtime");
 const XDate = require("xdate");
 
 const render_draft_table_body = require("../templates/draft_table_body.hbs");
diff --git a/static/js/filter.js b/static/js/filter.js
index e5461f15b0..d9768c8380 100644
--- a/static/js/filter.js
+++ b/static/js/filter.js
@@ -1,3 +1,4 @@
+const Handlebars = require("handlebars/runtime");
 const _ = require("lodash");
 
 const util = require("./util");
diff --git a/static/js/search_suggestion.js b/static/js/search_suggestion.js
index 24aed65337..d39aeeeace 100644
--- a/static/js/search_suggestion.js
+++ b/static/js/search_suggestion.js
@@ -1,3 +1,5 @@
+const Handlebars = require("handlebars/runtime");
+
 const huddle_data = require("./huddle_data");
 const settings_data = require("./settings_data");
 
diff --git a/static/js/templates.js b/static/js/templates.js
index a93fc79e7f..762312de78 100644
--- a/static/js/templates.js
+++ b/static/js/templates.js
@@ -1,3 +1,5 @@
+const Handlebars = require("handlebars/runtime");
+
 const util = require("./util");
 
 // Below, we register Zulip-specific extensions to the handlebars API.
diff --git a/static/js/typeahead_helper.js b/static/js/typeahead_helper.js
index c14d4f3c58..6d29acf065 100644
--- a/static/js/typeahead_helper.js
+++ b/static/js/typeahead_helper.js
@@ -1,3 +1,5 @@
+const Handlebars = require("handlebars/runtime");
+
 const pygments_data = require("../generated/pygments_data.json");
 const emoji = require("../shared/js/emoji");
 const typeahead = require("../shared/js/typeahead");
diff --git a/tools/webpack.assets.json b/tools/webpack.assets.json
index d199fd4aa8..edb6a875b2 100644
--- a/tools/webpack.assets.json
+++ b/tools/webpack.assets.json
@@ -8,7 +8,6 @@
     "archive": [
         "./static/js/bundles/portico.js",
         "katex/dist/katex.min.js",
-        "handlebars/dist/cjs/handlebars.runtime.js",
         "./static/js/archive.js",
         "./static/js/colorspace.js",
         "./static/js/floating_recipient_bar.js",
@@ -28,7 +27,6 @@
         "./static/styles/portico/landing-page.scss",
         "./static/js/billing/helpers.js",
         "./static/js/billing/billing.js",
-        "handlebars/dist/cjs/handlebars.runtime.js",
         "./static/js/templates.js",
         "./static/js/loading.js",
         "./static/styles/portico/billing.scss"
@@ -39,7 +37,6 @@
         "./static/styles/portico/landing-page.scss",
         "./static/js/billing/helpers.js",
         "./static/js/billing/upgrade.js",
-        "handlebars/dist/cjs/handlebars.runtime.js",
         "./static/js/templates.js",
         "./static/js/loading.js",
         "./static/styles/portico/billing.scss"
diff --git a/tools/webpack.config.ts b/tools/webpack.config.ts
index 44d6f42191..58bde4f359 100644
--- a/tools/webpack.config.ts
+++ b/tools/webpack.config.ts
@@ -246,7 +246,6 @@ export default (env?: string): webpack.Configuration[] => {
         {path: "./debug-require.js", name: "require"},
         {path: "../static/js/debug.js"},
         {path: "jquery/dist/jquery.js", name: ["$", "jQuery"]},
-        {path: "handlebars/dist/cjs/handlebars.runtime.js", name: "Handlebars"},
     ];
     config.module!.rules.unshift(...getExposeLoaders(exposeOptions));